Advertisement

Molecular Biology Reports

, Volume 45, Issue 6, pp 2897–2905 | Cite as

Plant stem cells: what we know and what is anticipated

  • Ashish R. WarghatEmail author
  • Kanika Thakur
  • Archit Sood
Review
  • 511 Downloads

Abstract

Plant stem cell research is of interest due to stem cells ability of unlimited division, therapeutic potential and steady supply to provide precursor cells. Their isolation and culture provides the important source for the production of homogenous lines of active constituents that allow large-scale production of various metabolites. The process of dedifferentiation and reversal to pluripotent cells involves the various pathways genes related to the stem cells and are associated to each other for maintaining a specific niche. Domains such as niche dynamics and maintenance signaling can be used for the identification of genes for stem cell niche. Significant findings have been achieved in the past on plant stem cells however our understanding towards mechanisms underlying some specific phenomenon like dedifferentiation, regulation, niche dynamics is still in infancy. The present review is based on the past research efforts and also pave a way forward for the future anticipation in the field of development of cell cultures for the production of active metabolites on large scale and undertanding transcriptional regulation of stem cell genes involved in niche signaling.

Keywords

Dedifferentiation DNA damage Genes Niche Plant stem cells Pluripotent 

Notes

Acknowledgements

The authors acknowledge the Council of Scientific and Industrial Research (CSIR), Government of India, under the project “Physiological, biochemical and molecular analysis of economically important plants for understanding and exploiting their growth, adaptation and metabolic mechanisms (MLP-0071)” for financial support. The authors are thankful to Director, CSIR-IHBT for providing necessary facilities.

Author Contributions

ARW—Conceived the concept, ARW & AS—Framed the design, ARW, KT & AS—Manuscript written and edition. All authors read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Ethical approval

Review article in accordance with ethical standard of institution.

References

  1. 1.
    Sablowski R (2004) Plant and animal stem cells: conceptually similar, molecularly distinct? Trends Cell Biol 14(11):605–611PubMedGoogle Scholar
  2. 2.
    Laux T (2003) The stem cell concept in plants: a matter of debate. Cell 113:281–283PubMedGoogle Scholar
  3. 3.
    Fulcher N, Sablowski R (2009) Hypersensitivity to DNA damage in plant stem cell niches. Proc Natl Acad Sci USA 106:20984–20988PubMedGoogle Scholar
  4. 4.
    Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057PubMedGoogle Scholar
  5. 5.
    Aichinger E, Kornet N, Friedrich T, Laux T (2012) Plant stem cell niches. Annu Rev Plant Biol 63:615–636PubMedPubMedCentralGoogle Scholar
  6. 6.
    Sozzani R, Iyer-Pascuzzi A (2014) Postembryonic control of root meristem growth and development. Curr Opin Plant Biol 17:7–12PubMedGoogle Scholar
  7. 7.
    Morus M, Baran M, Rost-Roszkowska M, Skotnicka-Graca U (2014) Plant stem cells as innovation in cosmetics. Acta Pol Pharm 71:701–707Google Scholar
  8. 8.
    Alison MR, Poulsom R, Forbes S, Wright NA (2002) An introduction to stem cells. J Pathol 197:419–423PubMedGoogle Scholar
  9. 9.
    Scheres B (2005) Stem cells: a plant biology perspective. Cell 122:499–504   PubMedGoogle Scholar
  10. 10.
    Gaillochet C, Lohmann JU (2015) The never-ending story: from pluripotency to plant developmental plasticity. Development 142:2237–2249PubMedPubMedCentralGoogle Scholar
  11. 11.
    Heidstra R, Sabatini S (2014) Plant and animal stem cells: similar yet different. Nat Rev Mol Cell Bio 15:301–312PubMedGoogle Scholar
  12. 12.
    Beeckman T, De Smet I (2014) Pericycle. Curr Biol 24:R378–R379PubMedGoogle Scholar
  13. 13.
    Sena G, Wang X, Liu HY, Hofhuis H, Birnbaum KD (2009) Organ regeneration does not require a functional stem cell niche in plants. Nature 457:1150–1153PubMedPubMedCentralGoogle Scholar
  14. 14.
    Sugimoto K, Gordon SP, Meyerowitz EM (2011) Regeneration in plants and animals: dedifferentiation, trans-differentiation, or just differentiation? Trends Cell Biol 21:212–218PubMedGoogle Scholar
  15. 15.
    Zhang W, Yu R (2014) Molecule mechanism of stem cells in Arabidopsis thaliana.  Pharmacogn Rev 8:105–112  PubMedPubMedCentralGoogle Scholar
  16. 16.
    Zhu J (2017) Plant stem cell and its pluripotency. Int J Stem Cell Res 3(1):001–006Google Scholar
  17. 17.
    Weigel D, Jurgens G (2002) Stem cells that make stems. Nature 415:751–754PubMedGoogle Scholar
  18. 18.
    Scofield S, Murray JA (2006) KNOX gene function in plant stem cell niches. Plant Mol Biol 60:929–946PubMedGoogle Scholar
  19. 19.
    Long JA, Barton MK (1998) The development of apical embryonic pattern in Arabidopsis. Development 125:3027–3035PubMedGoogle Scholar
  20. 20.
    Vernoux T, Benfey PN (2005) Signals that regulate stem cell activity during plant development. Curr Opin Genet Dev 15:388–394PubMedGoogle Scholar
  21. 21.
    Ueda M, Kimura YK, Okada K (2005) Stepwise understanding of root development. Curr Opin Plant Biol 8:71–76PubMedGoogle Scholar
  22. 22.
    Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh Y, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120PubMedGoogle Scholar
  23. 23.
    Verdeil JL, Alemanno L, Niemenak N, Tranbarger TJ (2007) Pluripotent versus totipotent plant stem cells: dependence versus autonomy? Trends Plant Sci 12:245–252PubMedGoogle Scholar
  24. 24.
    Gaj MD, Zhang S, Harada JJ, Lemaux PG (2005) Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222:977–988PubMedGoogle Scholar
  25. 25.
    Stone S, Kwong L, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98:11806–1181PubMedGoogle Scholar
  26. 26.
    Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, Van Lammeren Andre AM, Miki Brian LA, Custers Jan BM, Van Lookeren Campagne Michiel M (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749PubMedPubMedCentralGoogle Scholar
  27. 27.
    Ivanov VB (1986) Specific features of cell proliferation in plants with reference to the problem of stem cells. Tsitologiya 28:295–302Google Scholar
  28. 28.
    Ivanov VB, Dobrochaev AE, Baskin TI (2002) What the distribution of cell lengths in the root meristem does and does not reveal about cell division. J Plant Growth Regul 21:60–67PubMedGoogle Scholar
  29. 29.
    Barlow PW (1997) Stem cells and founder zones in plants, particularly their roots. In: Poten CS (ed) Stem cells. Academic, London, pp 29–57Google Scholar
  30. 30.
    Francis D (1997) The stem cell concept applied to shoot meristems of higher plants. In: Poten CS (ed) Stem cells. Academic, London, pp 59–73Google Scholar
  31. 31.
    Gross-Hardt R, Laux T (2003) Stem cell regulation in plant meristem. J Cell Sci 116(9):1659–1666PubMedGoogle Scholar
  32. 32.
    Clark SE (2001) Meristems: start your signaling. Curr Opin Plant Biol 4(1):28–32PubMedGoogle Scholar
  33. 33.
    Vagi P, Preininger E, Kovacs GM, Kristof Z, Boka K, Boddi B (2013) Structure of plants and fungi. In: Kristof Z (ed) Eötvös Loránd University, pp. 1–109Google Scholar
  34. 34.
    Rich T, Allen RL, Wyllie AH (2000) Defying death after DNA damage. Nature 407:777–783PubMedGoogle Scholar
  35. 35.
    Schumacher B, Hofmann K, Boulton S, Gartner A (2001) The C. elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis. Curr Biol 11:1722–1727PubMedGoogle Scholar
  36. 36.
    Vitale I, Maniac G, De Maria R, Kroemer G, Galluzzi L (2017) DNA damage in stem cells. Mol Cell 66(3):306–319PubMedGoogle Scholar
  37. 37.
    Klekowski E (2003) Plant clonality, mutation, diplontic selection and mutational meltdown. Biol J Linn Soc 79:61–67Google Scholar
  38. 38.
    Cools T, De Veylder L (2009) DNA stress checkpoint control and plant development. Curr Opin Plant Biol 12:23–28PubMedGoogle Scholar
  39. 39.
    Xu P, Yuan D, Liu M, Li C, Liu Y, Zhang S, Yao N, Yang C (2013) AtMMS21, an SMC5/6 complex subunit, is involved in stem cell niche maintenance and DNA damage responses in Arabidopsis roots. Plant Physiol 161:1755–1768PubMedPubMedCentralGoogle Scholar
  40. 40.
    Chavez A, George V, Agrawal V, Johnson FB (2010) Sumoylation and the structural maintenance of chromosomes (Smc) 5/6 complex slow senescence through recombination intermediate resolution. J Biol Chem 285:11922–11930PubMedPubMedCentralGoogle Scholar
  41. 41.
    Yoshiyama K (2015) SOG1: a master regulator of the DNA damage response in plants. Genes Genet Syst 90:209–216PubMedGoogle Scholar
  42. 42.
    Jamet E, Durr A, Parmentier Y, Criqui MC, Fleck J (1990) Is ubiquitin involved in the dedifferentiation of higher plant cells? Cell Differ Dev 29:37–46PubMedGoogle Scholar
  43. 43.
    Liu HL, Wang GC, Feng Z, Zhu J (2010) Screening of genes associated with dedifferentiation and effect of LBD29 on pericycle cells in Arabidopsis thaliana. Plant Growth Regul 62:127–136Google Scholar
  44. 44.
    Yadav RK, Tavakkoli M, Reddy GV (2010) WUSCHEL mediates stem cell homeostasis by regulating stem cell number and patterns of cell division and differentiation of stem cell progenitors. Development 137:3581–3589PubMedGoogle Scholar
  45. 45.
    Bell EM, Lin WC, Husbands AY, Yu L, Jaganatha V, Jablonska B, Mangeon Amanda, Neff MM, Girke T, Springer PS (2012) Arabidopsis lateral organ boundaries negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proc Natl Acad Sci USA 109:21146–21151PubMedGoogle Scholar
  46. 46.
    Reddy GV, Meyerowitz EM (2005) Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apex. Science 310:663–667PubMedGoogle Scholar
  47. 47.
    Koyama T, Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2010) TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 22:3574–3588PubMedPubMedCentralGoogle Scholar
  48. 48.
    Ikeda M, Ohme-Takagi M (2014) TCPs, WUSs, and WINDs: families of transcription factors that regulate shoot meristem formation, stem cell maintenance, and somatic cell differentiation. Front Plant Sci 5:427PubMedPubMedCentralGoogle Scholar
  49. 49.
    Liu H, Wang S, Yu X, Yu J, He X, Zhang S, Shou H, Wu P (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J 43:47–56PubMedGoogle Scholar
  50. 50.
    Iwase A, Ohme-Takagi M, Sugimoto K (2011) WIND1: A key molecular switch for plant cell dedifferentiation. Plant Signal Behav 6:1943–1945PubMedPubMedCentralGoogle Scholar
  51. 51.
    Zhou C, Guo J, Feng Z, Cui X, Zhu J (2012) Molecular characterization of a novel AP2 transcription factor ThWIND1-L from Thellungiella halophila. Plant Cell Tiss Org 110:423–433Google Scholar
  52. 52.
    Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7:e1002243PubMedPubMedCentralGoogle Scholar
  53. 53.
    Li F, Cui X, Feng Z, Du X, Zhu J (2012) The effect of 2,4-D and kinetin on differentiation of petiole cells in Arabidopsis thaliana. Biol Plantarum 56:121–125Google Scholar
  54. 54.
    Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fakuda H (2006) Dodeca-CLE peptides as suppressors of plant stem differentiation. Science 313:8842–8845Google Scholar
  55. 55.
    Grafi G (2004) How cells dedifferentiate: a lesson from plants. Dev Biol 268:1–6PubMedGoogle Scholar
  56. 56.
    Cai S, Fu XB, Sheng ZY (2007) Dedifferentiation: a new approach in stem cell research. Bioscience 57:655–662Google Scholar
  57. 57.
    Scheres B (2007) Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol 8:345–354PubMedGoogle Scholar
  58. 58.
    Mayer KFX, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815PubMedGoogle Scholar
  59. 59.
    Song SK, Lee MM, Clark SE (2006) POLK and PLL1 phosphatases are CLAVATA1 signaling intermediates required for Arabidopsis shoot and floral stem cells. Development 133: 4691–4698PubMedGoogle Scholar
  60. 60.
    Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol 5:578–580PubMedGoogle Scholar
  61. 61.
    Yadav RK, Perales M, Gruel J, Ohno C, Heisler M et al (2013) Plant stem cell maintenance involves direct transcriptional repression of differentiation program. Mol Syst Biol 9:1–13Google Scholar
  62. 62.
    Busch W, Miotk A, Ariel FD, Zhao Z, Forner J, Daum G, Suzaki T, Schuster C, Schultheiss SJ, Leibfried A, Haubeiss S, Ha N, Chan RL, Lohmann JU (2010) Transcriptional control of a plant stem cell niche. Dev Cell 18:849–861PubMedGoogle Scholar
  63. 63.
    Lohmann J, Huong R, Hobe M, Busch M, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803PubMedGoogle Scholar
  64. 64.
    Ji J, Strable J, Shimizu R, Koenig D, Sinha N, Scanlon MJ (2010) WOX4 promotes procambial development. Plant Physiol 152:1346–1356PubMedGoogle Scholar
  65. 65.
    Kamiya N, Nagasaki H, Morikami A, Sato Y, Matsuoka M (2003) Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. Plant J 35:429–441PubMedGoogle Scholar
  66. 66.
    Nardmann J, Zimmermann R, Durantini D, Kranz E, Werr W (2007) WOX gene phylogeny in Poaceae: a comparative approach addressing leaf and embryo development. Mol Biol Evol 24:2474–2484PubMedGoogle Scholar
  67. 67.
    Guo Y, Han L, Hymes M, Denver R, Clark SE (2010) CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J 63:889–900PubMedPubMedCentralGoogle Scholar
  68. 68.
    Schuster C, Gailochet C, Lohmann JU (2015) Arabidopsis HECATE genes function in phytohormone control during gynoecium development. Development 142:3343–3350PubMedPubMedCentralGoogle Scholar
  69. 69.
    Scofield S, Dewitte W, Murray JA (2014) STM sustains stem cell function in the Arabidopsis shoot apical meristem and controls KNOX gene expression independently of the transcriptional repressor AS1. Plant Signal Behav 9:e28934PubMedPubMedCentralGoogle Scholar
  70. 70.
    Yadav RK, Girke T, Pasala S, Xie M, Reddy GV (2009) Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc Nat Acad Sci USA 106:4941–4946PubMedGoogle Scholar
  71. 71.
    Zhao J, Morozova N, Williams L, Libs L, Avivi Y, Grafi G (2001) Two phases of chromatin de-condensation during dedifferentiation of plant cells: distinction between competence for cell fate switch and a commitment for S phase. J Biol Chem 276:22772–22778PubMedGoogle Scholar
  72. 72.
    Meshorer E, Misteli T (2006) Chromatin in pluripotent embryonic stem cells and differentiation. Nat Rev Mol Cell Biol 7:540–546PubMedGoogle Scholar
  73. 73.
    Tessadori F, Chupeau MC, Chupeau Y, Knip M, Germann S, Van Driel R, Fransz P, Gaudin V (2007) Large-scale dissociation and sequential reassembly of pericentric heterochromatin in dedifferentiated Arabidopsis cells. J Cell Sci 120:1200–1120PubMedGoogle Scholar
  74. 74.
    Grafi G, Ben-Meir H, Avivi Y, Moshe M, Dahan Y, Zemach A (2007) Histone methylation controls telomerase-independent telomere lengthening in cells undergoing dedifferentiation. Dev Biol 306:838–846PubMedGoogle Scholar
  75. 75.
    Jiang F, Zhu J, Liu HL (2013) Protoplasts: a useful research system for plant cell biology, especially dedifferentiation. Protoplasma 250:1231–1238PubMedGoogle Scholar
  76. 76.
    Chan SW, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6:351–360PubMedGoogle Scholar
  77. 77.
    Desvoyes B, Sanchez MP, Ramirez-Parra E, Gutierrez C (2010) Impact of nucleosome dynamics and histone modifications on cell proliferation during Arabidopsis development. Heredity (Edinb.) 105:80–91Google Scholar
  78. 78.
    Lee EK, Jin YW, Park JH, et al (2010) Cultured cambial meristematic cells as a source of plant natural products. Nat Biotechnol 28:1213–1217PubMedGoogle Scholar
  79. 79.
    Ochoa-Villarreal M, Howat S, Jang MO, Kim IS, Jin Y-W, Lee E-K, et al (2015) Cambial meristematic cells: a platform for the production of plant natural products. New Biotechnol 32(6):581–587Google Scholar
  80. 80.
    Jang SH, Yu JY, Lee EK, Lim MJ, Hong NJ, Oh IS, Kang TH, So EM, Jin YW, Jin YS, Jeong YS, Jeong HS, Lee JC, Jang YS (2012) In vitro anti-oxidant and anti-inflammatory activities of cambial meristematic cells established from Ginkgo biloba L. J Med Plants Res 6:3048–3058Google Scholar
  81. 81.
    http://www.ulprospector.com/. Accessed 21 Aug 2018
  82. 82.
    Moon SH, Venkatesh J, Yu JW, Park SW (2015) Differential induction of meristematic stem cells of Catharanthus roseus and their characterization. C R Biol 338:745–756PubMedGoogle Scholar
  83. 83.
    Croteau R, Ketchum REB, Long RM, Kaspera R, Wildung MR (2006) Taxol biosynthesis and molecular genetics. Phytochem Rev 5:75–97PubMedPubMedCentralGoogle Scholar
  84. 84.
    Roberts SC (2007) Production and engineering of terpenoids in plant cell culture. Nat Chem Biol 3:387–395PubMedGoogle Scholar
  85. 85.
    Barbulova A, Fabio A, Gabriella C (2014) Plant cell cultures as source of cosmetic active ingredients. Cosmetics 1(2):94–104Google Scholar
  86. 86.
    Tomlinson PB, Huggett BA (2012) Cell longevity and sustained primary growth in palm stems. Am J Bot 99:1891–1902PubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Ashish R. Warghat
    • 1
    Email author
  • Kanika Thakur
    • 1
  • Archit Sood
    • 1
  1. 1.Biotechnology DivisionCSIR-Institute of Himalayan Bioresource TechnologyPalampurIndia

Personalised recommendations