Advertisement

Science Bulletin

, Volume 61, Issue 11, pp 847–858 | Cite as

Stem cell lineage in body layer specialization and vascular patterning of rice root and leaf

  • Minhuan Zeng
  • Bo Hu
  • Jiqin Li
  • Guifang Zhang
  • Ying Ruan
  • Hai Huang
  • Hua Wang
  • Lin Xu
Article Life & Medical Sciences

Abstract

Since the first appearance of vascular plants during evolution, the plant body has become specialized for adaption to land conditions. Much of our knowledge of plant body specialization and the origins of tissues from stem cells have been obtained from studies on the dicot Arabidopsis thaliana. However, less is known about plant body specialization in monocots, another important branch of angiosperms. In this study, we analyzed stem cell lineage and differentiation during development of the root and leaf of the monocot model plant rice (Oryza sativa). Our results showed that three body layers of rice are established from stem cells accompanied by progressively reduced pluripotency. Layer 1 (L1) is a single-cell layer of epidermis; L2 is the cortex/endodermis in the root and the mesophyll in the leaf; and L3 is the site of vascular initiation. At least two common steps in vascular development are shared between rice root and leaf. The preprocambium divides to form the procambium and root pericycle or leaf outer sheath. The procambium further differentiates into the xylem, phloem and circumambient cells. We found that the outer sheath of leaf vascular bundles originates not only from the preprocambium of L3, but also from the mesophyll precursor cells of L2. In addition, WUSCHEL-RELATED HOMEOBOX (WOX) genes are expressed in not only the stem cell niche but also metaxylem precursor in rice. This pattern differs from that of homologs in Arabidopsis, suggesting that WOX functions have been recruited in different stem cells in dicots and monocots.

Keywords

Oryza sativa Stem cell Body layer Preprocambium Vascular development WOX 

Notes

Acknowledgments

This work was supported by National Basic Research Program of China (2014CB943500/2012CB910500), the National Natural Science Foundation of China (91419302/31422005) and Youth Innovation Promotion Association of Chinese Academy of Sciences. We thank Y. Guan for critical reading of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Scarpella E, Meijer AH (2004) Pattern formation in the vascular system of monocot and dicot plant species. New Phytol 164:209–242CrossRefGoogle Scholar
  2. 2.
    Bennici A (2007) Unresolved problems on the origin and early evolution of land plants. Riv Biol 100:55–67Google Scholar
  3. 3.
    Bennici A (2008) Origin and early evolution of land plants: problems and considerations. Commun Integr Biol 1:212–218CrossRefGoogle Scholar
  4. 4.
    Coudert Y, Perin C, Courtois B et al (2010) Genetic control of root development in rice, the model cereal. Trends Plant Sci 15:219–226CrossRefGoogle Scholar
  5. 5.
    Elo A, Immanen J, Nieminen K et al (2009) Stem cell function during plant vascular development. Semin Cell Dev Biol 20:1097–1106CrossRefGoogle Scholar
  6. 6.
    Miyashima S, Sebastian J, Lee JY et al (2013) Stem cell function during plant vascular development. EMBO J 32:178–193CrossRefGoogle Scholar
  7. 7.
    Xu L, Huang H (2014) Genetic and epigenetic controls of plant regeneration. Curr Top Dev Biol 108:1–33CrossRefGoogle Scholar
  8. 8.
    Scheres B (2007) Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol 8:345–354CrossRefGoogle Scholar
  9. 9.
    Aichinger E, Kornet N, Friedrich T et al (2012) Plant stem cell niches. Annu Rev Plant Biol 63:615–636CrossRefGoogle Scholar
  10. 10.
    Lander AD (2009) The “stem cell” concept: is it holding us back? J Biol 8:70CrossRefGoogle Scholar
  11. 11.
    Jaenisch R, Young R (2008) Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132:567–582CrossRefGoogle Scholar
  12. 12.
    Haecker A, Gross-Hardt R, Geiges B et al (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–668CrossRefGoogle Scholar
  13. 13.
    van der Graaff E, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10:248CrossRefGoogle Scholar
  14. 14.
    Zhang X, Zong J, Liu J et al (2010) Genome-wide analysis of WOX gene family in rice, sorghum, maize, Arabidopsis and poplar. J Integr Plant Biol 52:1016–1026CrossRefGoogle Scholar
  15. 15.
    Nardmann J, Werr W (2012) The invention of WUS-like stem cell-promoting functions in plants predates leptosporangiate ferns. Plant Mol Biol 78:123–134CrossRefGoogle Scholar
  16. 16.
    Lian G, Ding Z, Wang Q et al (2014) Origins and evolution of WUSCHEL-related homeobox protein family in plant kingdom. Sci World J 2014:534140CrossRefGoogle Scholar
  17. 17.
    Mukherjee K, Brocchieri L, Burglin TR (2009) A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol Biol Evol 26:2775–2794CrossRefGoogle Scholar
  18. 18.
    Zeng L, Zhang Q, Sun R et al (2014) Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times. Nat Commun 5:4956CrossRefGoogle Scholar
  19. 19.
    Rost TL, Barbour MG, Stocking CR et al (1997) Plant biology. Wadsworth Publishing Company, Belmont, California, USAGoogle Scholar
  20. 20.
    Rebouillat J, Dievart A, Verdeil JL et al (2009) Molecular genetics of rice root development. Rice 2:15–34CrossRefGoogle Scholar
  21. 21.
    Itoh J, Nonomura K, Ikeda K et al (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47CrossRefGoogle Scholar
  22. 22.
    Xu L, Xu Y, Dong A et al (2003) Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development 130:4097–4107CrossRefGoogle Scholar
  23. 23.
    Liu J, Sheng L, Xu Y et al (2014) WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell 26:1081–1093CrossRefGoogle Scholar
  24. 24.
    Chen X, Qu Y, Sheng L et al (2014) A simple method suitable to study de novo root organogenesis. Front Plant Sci 5:208CrossRefGoogle Scholar
  25. 25.
    Li H, Xu L, Wang H et al (2005) The Putative RNA-dependent RNA polymerase RDR6 acts synergistically with ASYMMETRIC LEAVES1 and 2 to repress BREVIPEDICELLUS and MicroRNA165/166 in Arabidopsis leaf development. Plant Cell 17:2157–2171CrossRefGoogle Scholar
  26. 26.
    Yao X, Huang H, Xu L (2012) In situ detection of mature miRNAs in plants using LNA-modified DNA probes. Methods Mol Biol 883:143–154CrossRefGoogle Scholar
  27. 27.
    He C, Chen X, Huang H et al (2012) Reprogramming of H3K27me3 is critical for acquisition of pluripotency from cultured Arabidopsis tissues. PLoS Genet 8:e1002911CrossRefGoogle Scholar
  28. 28.
    Kamiya N, Nagasaki H, Morikami A et al (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 35:429–441CrossRefGoogle Scholar
  29. 29.
    Wang L, Chu H, Li Z et al (2014) Origin and development of the root cap in rice. Plant Physiol 166:603–613CrossRefGoogle Scholar
  30. 30.
    Bennett T, Scheres B (2010) Root development-two meristems for the price of one? Curr Top Dev Biol 91:67–102CrossRefGoogle Scholar
  31. 31.
    De Rybel B, Breda AS, Weijers D (2013) Prenatal plumbing–vascular tissue formation in the plant embryo. Physiol Plant 151:126–133CrossRefGoogle Scholar
  32. 32.
    Clark LH, Harris WH (1981) Observations on the root anatomy of rice (Oryza sativa L.). Am J Bot 68:154CrossRefGoogle Scholar
  33. 33.
    Hochholdinger F, Park WJ, Sauer M et al (2004) From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci 9:42–48CrossRefGoogle Scholar
  34. 34.
    Orman-Ligeza B, Parizot B, Gantet PP et al (2013) Post-embryonic root organogenesis in cereals: branching out from model plants. Trends Plant Sci 18:459–467CrossRefGoogle Scholar
  35. 35.
    Casero PJ, Casimiro I, Lloret PG (1995) Lateral root initiation by asymmetrical transverse divisions of pericycle cells in four plant species: Raphanus sativus, Helianthus annuus, Zea mays, and Daucus carota. Protoplasma 188:49–58CrossRefGoogle Scholar
  36. 36.
    Demchenko NP, Demchenko KN (2001) Resumption of DNA synthesis and cell division in wheat roots as related to lateral root initiation. Russ J Plant Physiol 48:755–764CrossRefGoogle Scholar
  37. 37.
    Hagemann W, Gleissberg S (1996) Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms. Pl Syst Evol 199:121–152CrossRefGoogle Scholar
  38. 38.
    Nardmann J, Ji J, Werr W et al (2004) The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 131:2827–2839CrossRefGoogle Scholar
  39. 39.
    Shimizu R, Ji J, Kelsey E et al (2009) Tissue specificity and evolution of meristematic WOX3 function. Plant Physiol 149:841–850CrossRefGoogle Scholar
  40. 40.
    Nakata M, Matsumoto N, Tsugeki R et al (2012) Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell 24:519–535CrossRefGoogle Scholar
  41. 41.
    Martins S, Scatena VL (2011) Bundle sheath ontogeny in Kranz and non-Kranz species of Cyperaceae (Poales). Aust J Bot 59:554–562CrossRefGoogle Scholar
  42. 42.
    Nardmann J, Reisewitz P, Werr W (2009) Discrete shoot and root stem cell-promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Mol Biol Evol 26:1745–1755CrossRefGoogle Scholar
  43. 43.
    Deveaux Y, Toffano-Nioche C, Claisse G et al (2008) Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evol Biol 8:291CrossRefGoogle Scholar
  44. 44.
    Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163CrossRefGoogle Scholar
  45. 45.
    Cho SH, Yoo SC, Zhang H et al (2013) The rice narrow leaf2 and narrow leaf3 loci encode WUSCHEL-related homeobox 3A (OsWOX3A) and function in leaf, spikelet, tiller and lateral root development. New Phytol 198:1071–1084CrossRefGoogle Scholar
  46. 46.
    Ishiwata A, Ozawa M, Nagasaki H et al (2013) Two WUSCHEL-related homeobox genes, narrow leaf2 and narrow leaf3, control leaf width in rice. Plant Cell Physiol 54:779–792CrossRefGoogle Scholar
  47. 47.
    Matsumoto N, Okada K (2001) A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev 15:3355–3364CrossRefGoogle Scholar
  48. 48.
    Sarkar AK, Luijten M, Miyashima S et al (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814CrossRefGoogle Scholar
  49. 49.
    Chu H, Liang W, Li J et al (2013) A CLE-WOX signalling module regulates root meristem maintenance and vascular tissue development in rice. J Exp Bot 64:5359–5369CrossRefGoogle Scholar
  50. 50.
    Cui H, Hao Y, Kovtun M et al (2011) Genome-wide direct target analysis reveals a role for SHORT-ROOT in root vascular patterning through cytokinin homeostasis. Plant Physiol 157:1221–1231CrossRefGoogle Scholar
  51. 51.
    Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22:2618–2629CrossRefGoogle Scholar
  52. 52.
    Ji J, Strable J, Shimizu R et al (2010) WOX4 promotes procambial development. Plant Physiol 152:1346–1356CrossRefGoogle Scholar
  53. 53.
    Ohmori Y, Tanaka W, Kojima M et al (2013) WUSCHEL-RELATED HOMEOBOX4 is involved in meristem maintenance and is negatively regulated by the CLE gene FCP1 in rice. Plant Cell 25:229–241CrossRefGoogle Scholar
  54. 54.
    Hanstein J (1868) Die scheitelzellgrouppe im vegetationspunkt der phanerogamen. Festschr Niederrhein Ges Natur u Heilk 109–134Google Scholar
  55. 55.
    Solnica-Krezel L, Sepich DS (2012) Gastrulation: making and shaping germ layers. Annu Rev Cell Dev Biol 28:687–717CrossRefGoogle Scholar
  56. 56.
    Elo A, Immanen J, Nieminen K et al (2009) Stem cell function during plant vascular development. Semin Cell Dev Biol 20:1097–1106CrossRefGoogle Scholar
  57. 57.
    Heyman J, Cools T, Vandenbussche F et al (2013) ERF115 controls root quiescent center cell division and stem cell replenishment. Science 342:860–863CrossRefGoogle Scholar
  58. 58.
    Sugimoto K, Gordon SP, Meyerowitz EM (2011) Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation? Trends Cell Biol 21:212–218CrossRefGoogle Scholar
  59. 59.
    Nardmann J, Werr W (2013) Symplesiomorphies in the WUSCHEL clade suggest that the last common ancestor of seed plants contained at least four independent stem cell niches. New Phytol 199:1081–1092CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.National Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological SciencesChinese Academy of SciencesShanghaiChina
  2. 2.Hunan Provincial Key Laboratory of Crop Germplasm Innovation and UtilizationHunan Agricultural UniversityChangshaChina

Personalised recommendations