Advertisement

Journal of Plant Biology

, Volume 61, Issue 6, pp 358–365 | Cite as

Stem Cell Maintenance and Abiotic Stress Response in Shoot Apical Meristem for Developmental Plasticity

  • Horim LeeEmail author
Review Article

Abstract

The shoot apical meristem (SAM) serves as a non-drying reservoir of pluripotent stem cells to supply new daughter cells forming above-ground tissues and organs such as leaves, stems, flowers and fruits throughout the life cycle of plants. Accordingly, the homeostasis control of stem cell division and differentiation must be an essential core mechanism for harmonic growth and development of plants as multicellular higher eukaryotes. Unlike animals, plants are sessile organisms and thus constantly face environmental factors, including abiotic stresses. Therefore, post-embryonic development derived from stem cells in the SAM likely interacts with surrounding abiotic stresses for plant adaptation and plastic development. For this reason, this review provides the most recent findings regarding comprehensive signaling networks involved in stem cell maintenance in the SAM, and then describes how stem cell signaling is related with abiotic stress response through involvement of phytohormones and reactive oxygen species in the SAM.

Keywords

Abiotic stress Differentiation Plasticity Reactive Oxygen species (ROS) SAM development Stem Cell Proliferation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aichinger E, Kornet N, Friedrich T, Laux T (2012) Plant stem cell niches. Annu Rev Plant Biol 63:615–636CrossRefGoogle Scholar
  2. Aida M, Ishida T, Tasaka M (1999) Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUC-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126:1563–1570Google Scholar
  3. Avramova Z (2015) Transcriptional ‘memory’ of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J 83:149–159CrossRefGoogle Scholar
  4. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240CrossRefGoogle Scholar
  5. Beckers GJM, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:944–953CrossRefGoogle Scholar
  6. Betsuyaku S, Takahashi F, Kinoshita A, Miwa H, Shinozaki K, Fukuda H, Sawa S (2011) Mitogen-activated protein kinase regulated by the CLAVATA receptors contributes to shoot apical meristem homeostasis. Plant Cell Physiol 52:14–29CrossRefGoogle Scholar
  7. Bommert P, Je BI, Goldshmidt A, Jackson D (2013) The maize Ga gene COMPACT PLANT2 functions in CLAVATA signalling to control shoot meristem size. Nature 502:555–558CrossRefGoogle Scholar
  8. Bowman JL, Eshed Y (2000) Formation and maintenance of the shoot apical meristem. Trends Plant Sci 5:110–115CrossRefGoogle Scholar
  9. Chou H, Zhu Y, Ma Y, Berkowitz GA (2016) The CLAVATA signaling pathway mediating stem cell fate in shoot meristems requires Ca2+ as a secondary cytosolic messenger. Plant J 85:494–506CrossRefGoogle Scholar
  10. Clark SE, Running MP, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119:397–418Google Scholar
  11. Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585CrossRefGoogle Scholar
  12. Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ (2016) Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv 2:e1501340CrossRefGoogle Scholar
  13. Damri M, Grano G, Ben-Meir H, Avivi Y, Plaschkes I, Chalifa-Caspi V, Wolfson M, Fraifeld V, Grafi G (2009) Senescing cells share common features with dedifferentiating cells. Rejuvenation Res 12:435–443CrossRefGoogle Scholar
  14. DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J 45:1–16CrossRefGoogle Scholar
  15. Dolzblasz A, Smakowska E, Gola EM, Sokolowska K, Kicia M, Janska H (2016) The mitochondrial protease AtFTSH4 safeguards Arabidopsis shoot apical meristem function. Sci Rep 6:28315CrossRefGoogle Scholar
  16. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristem. Science 283:1911–1914CrossRefGoogle Scholar
  17. Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM (2009) Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc Natl Acad Sci USA 106:16529–16532CrossRefGoogle Scholar
  18. Grafi G, Chalifa-Caspi V, Nagar T, Plaschkes I, Barak S, Ransbotyn V (2011a) Plant response to stress meets dedifferentiation. Planta 233:433–438CrossRefGoogle Scholar
  19. Grafi G, Florentin A, Ransbotyn V, Morgenstern Y (2011b) The stem cell state in plant development and in response to stress. Front Plant Sci 2:53CrossRefGoogle Scholar
  20. 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 63:889–900CrossRefGoogle Scholar
  21. Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17:172–179CrossRefGoogle Scholar
  22. Hamanaka RB, Glasauer A, Hoover P, Yang SN, Blatt H, Mullen AR, Getsios S, Gottardi CJ, DeBerardinis RJ, Lavker RM, Chandel NS (2013) Mitochondrial reactive oxygen species promote epidermal epidermal differentiation and hair follicle development. Sci Signal 6:ra8CrossRefGoogle Scholar
  23. Haswell ES, Meyerowitz EM (2006) MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr Biol 16:1–11CrossRefGoogle Scholar
  24. Hu C, Zhu Y, Cui Y, Cheng K, Liang W, Wei Z, Zhu M, Yin H, Zeng L, Xiao Y, Lv M, Yi J, Hou S, He K, Li J, Gou X (2018) A group of receptor kinases are essential for CLAVATA signalling to maintain stem cell homeostasis. Nat Plants 4:205–211CrossRefGoogle Scholar
  25. Hwang I, Sheen J, Müller B (2012) Cytokinin signaling networks. Annu Rev Plant Biol 63:353–380CrossRefGoogle Scholar
  26. Ishida T, Tabata R, Yamada M, Aida M, Mitsumasu K, Fujiwara M, Yamaguchi K, Shigenobu S, Higuchi M, Tsuji H, Shimamoto K, Hasebe M, Fukuda H, Sawa S (2014) Heterotrimeric G proteins control stem cell proliferation through CLAVATA signaling in Arabidopsis. EMBO Rep 15:1202–1209CrossRefGoogle Scholar
  27. Jalmi SK, Sinha AK (2015) ROS mediated MAPK signaling in abiotic and biotic stress-strikng similarities and differences. Front Plant Sci 6:769CrossRefGoogle Scholar
  28. Jeon J, Kim NY, Kim S, Kang NY, Novák O, Ku SJ, Cho C, Lee KJ, Lee EJ, Strnad M, Kim J (2010) A subset of cytokinin twocomponent signaling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem 285:23371–23386CrossRefGoogle Scholar
  29. Jeong S, Trotochaud AE, Clark SE (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11:1925–1933CrossRefGoogle Scholar
  30. Kayes JM, Clark SE (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125:3843–3851Google Scholar
  31. Kimura Y, Tasaka M, Torii KU, Uchida N (2017) ERECTA-family genes coordinate stem cell functions between the epidermal and internal layers of the shoot apical meristem. Development 145:dev156380CrossRefGoogle Scholar
  32. Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, Stahl Y, Simon R, Yamaguchi-Shinozaki K, Fukuda H, Sawa S (2010) RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137:3911–3920CrossRefGoogle Scholar
  33. Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H, Sakagami Y (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF analysis. Science 313:845–848CrossRefGoogle Scholar
  34. Laux T, Mayer KFX, Berger J, Jürgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96Google Scholar
  35. Lee C, Clark SE (2015) A WUSHCEL-independent stem cell specification pathway is repressed by PHB, PHV and CNA in Arabidopsis. PLoS ONE 10:e0126006CrossRefGoogle Scholar
  36. Lee HG, Choi YR, Seo PJ (2016) Increased STM expression is associated with drought tolerance in Arabidopsis. J Plant Physiol 201:79–87CrossRefGoogle Scholar
  37. Long JA, Barton MK (1998) The development of apical embryonic pattern in Arabidopsis. Development 125:3027–3035Google Scholar
  38. Malinska D, Kudin AP, Bejtka M, Kunz WS (2012) Changes in mitochondrial reactive oxygen species synthesis during differentiation of skeletal muscle cells. Mitochondrion 12:144–148CrossRefGoogle Scholar
  39. Mandel T, Candela H, Landau U,Asis L,ZelingerE, Carles CC, Williams LE (2016) Differential regulation of meristem size, morphology and organization by the ERECTA, CLAVATA and class III HD-ZIP pathways. Development 143:1612–1622CrossRefGoogle Scholar
  40. 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 95:805–815CrossRefGoogle Scholar
  41. Müller R, Bleckmann A, Simon R (2008) The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20:934–946CrossRefGoogle Scholar
  42. Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T, Sakakibara H, Schmülling T, Tran LS (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23:2169–2183CrossRefGoogle Scholar
  43. O'Brien J, Benková E (2013) Cytokinin cross-talking during biotic and abiotic stress responses. Front Plant Sci 4:451Google Scholar
  44. Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol 5:578–580CrossRefGoogle Scholar
  45. Pasternak T, Rudas V, Potters G, Jansen MAK (2005) Morphogenic effects of abiotic stress: reorientation of growth in Arabidopsis thaliana seedlings. Environ Exp Bot 53:299–314CrossRefGoogle Scholar
  46. Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends in Plant Sci 12:98–105CrossRefGoogle Scholar
  47. Reddy GV, Meyerowitz EM (2005) Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apex. Science 310:663–667CrossRefGoogle Scholar
  48. Rodriguez MCS, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649CrossRefGoogle Scholar
  49. Sablowsk R (2007) The dynamic plant stem cell niches. Curr Opin Plant Biol 10:639–644CrossRefGoogle Scholar
  50. Schulze S, Schäfer BN, Parizotto EA, Voinnet O, Theres K (2010) LOST MERISTEMS genes regulate cell differentiation of central zone descendants in Arabidopsis shoot meristems. Plant J 64:668–678CrossRefGoogle Scholar
  51. Scofield S, Murison A, Jones A, Fozard J, Aida M, Band LR, Bennett M, Murray JAH (2018) Coordination of meristem and boundary functions by transcription factors in the SHOOT MERISTEMLESS regulatory network. Development 145:dev157081CrossRefGoogle Scholar
  52. Shinohara H, Matsubayashi Y (2015) Reevaluation of the CLV3-receptor interaction in the shoot apical meristem: dissection of the CLV3 signaling pathway from a direct ligand-binding point of view. Plant J 82:328–336CrossRefGoogle Scholar
  53. Sinha AK, Jaggi M, Raghuram B, Tuteja N (2011) Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal Behav 6:2CrossRefGoogle Scholar
  54. Somssich M, Je BI, Simon R, Jackson D (2016) CLAVATA-WUSCHEL signaling in the shoot meristem. Development 143:3238–3248CrossRefGoogle Scholar
  55. Soyars CL, James SR, Nimchuk ZL (2016) Ready, aim, shoot: stem cell regulation of the shoot apical meristem. Curr Opin Plant Biol 29:163–168CrossRefGoogle Scholar
  56. Sung S, Amaino RM (2005) Remembering winter: toward a molecular understanding of vernalization. Annu Rev Plant Biol 56:491–508CrossRefGoogle Scholar
  57. Takada S, Hibara K, Ishida T, Tasaka M (2001) The CUC-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128:1127–1135Google Scholar
  58. Tran LS, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104:20623–20628CrossRefGoogle Scholar
  59. Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550CrossRefGoogle Scholar
  60. Wilson ME, Jensen GS, Haswell ES (2011) Two mechanosensitive channel homologs influence division ring placement in Arabidopsis chloroplasts. Plant Cell 23:2939–2949CrossRefGoogle Scholar
  61. Wilson ME, Mixdorf M, Berg RH, Haswell ES (2016) Plastid osmotic stress influences cell differentiation at the plant shoot apex. Development 143:3382–3393CrossRefGoogle Scholar
  62. Yadav RK, Girke T, Pasala S, Xie M, Reddy GV (2009) Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc Natl Acad Sci USA 106:4941–4946CrossRefGoogle Scholar
  63. Yadav RK, Perales M, Gruel J, Girke T, Jönsson H, Reddy GV (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25:2025–2030CrossRefGoogle Scholar
  64. Yanai O, Shani E, Dolezal K, Tarkowsk P, Sablowski R, Sandberg G, Samach A, Ori N (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol 15:1566–1571CrossRefGoogle Scholar
  65. Zhou Y, Liu X, Engstrom EM, Nimchuk ZL, Pruneda-Paz JL, Tarr PT, Yan A, Kay SA, Meyerowitz EM (2015) Control of plant stem cell function by conserved interacting transcriptional regulators. Nature 517:377–380CrossRefGoogle Scholar
  66. Zhou Y, Yan A, Han H, Li T, Geng Y, Liu X, Meyerowitz EM (2018) HAIRY MERISTEM with WUSCHEL confines CLAVATA3 expression to the outer apical meristem layers. Science 361:502–506CrossRefGoogle Scholar
  67. Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324CrossRefGoogle Scholar
  68. Zeng J, Dong Z, Wu H, Tian Z, Zhao Z (2017) Redox regulation of plant stem cell fate. EMBO J 36:2844–2855CrossRefGoogle Scholar

Copyright information

© Korean Society of Plant Biologists and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiotechnologyDuksung Women’s UniversitySeoulKorea

Personalised recommendations