APL regulates vascular tissue identity in Arabidopsis

Abstract

Vascular plants have a long-distance transport system consisting of two tissue types with elongated cell files, phloem and xylem1. Phloem has two basic cell types, enucleate sieve elements and companion cells. Xylem has various lignified cell types, such as tracheary elements, the differentiation of which involves deposition of elaborate cell wall thickenings and programmed cell death1,2,3,4. Until now, little has been known about the genetic control of phloem–xylem patterning. Here we identify the ALTERED PHLOEM DEVELOPMENT (APL) gene, which encodes a MYB coiled-coil-type transcription factor that is required for phloem identity in Arabidopsis. Phloem is established through asymmetric cell divisions and subsequent differentiation. We show that both processes are impaired by a recessive apl mutation. This is associated with the formation of cells that have xylem characteristics in the position of phloem. The APL expression profile is consistent with a key role in phloem development. Ectopic APL expression in the vascular bundle inhibits xylem development. Our studies suggest that APL has a dual role both in promoting phloem differentiation and in repressing xylem differentiation during vascular development.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: apl has an altered vascular pattern.
Figure 2: Asymmetric cell divisions, SE and CC differentiation are defective in apl.
Figure 3: Molecular characterization of the APL locus.
Figure 4: Ectopic APL expression inhibits xylem differentiation.

References

  1. 1

    Esau, K. Anatomy of Seed Plants 2nd edn (John Wiley & Sons, New York, 1977)

    Google Scholar 

  2. 2

    Oparka, K. J. & Turgeon, R. Sieve elements and companion cells—traffic control centers of the phloem. Plant Cell 11, 739–750 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  3. 3

    Kuhn, C. et al. Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275, 1298–1300 (1997)

    CAS  Article  Google Scholar 

  4. 4

    Ye, Z. H. Vascular tissue differentiation and pattern formation in plants. Annu. Rev. Plant Biol. 53, 183–202 (2002)

    CAS  Article  Google Scholar 

  5. 5

    McConnell, J. R. & Barton, M. K. Leaf polarity and meristem formation in Arabidopsis. Development 125, 2935–2942 (1998)

    CAS  Google Scholar 

  6. 6

    Waites, R. & Hudson, A. phantastica: a gene required for dorsiventrality of leaves in Antirrhinum majus. Development 121, 2143–2154 (1995)

    CAS  Google Scholar 

  7. 7

    Aloni, R. Differentiation of vascular tissues. Annu. Rev. Plant Physiol. 38, 179–204 (1987)

    Article  Google Scholar 

  8. 8

    Carland, F. M. et al. Genetic regulation of vascular tissue patterning in Arabidopsis. Plant Cell 11, 2123–2137 (1999)

    CAS  Article  Google Scholar 

  9. 9

    Mahonen, A. P. et al. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev. 14, 2938–2943 (2000)

    CAS  Article  Google Scholar 

  10. 10

    Baum, S. F., Dubrovsky, J. G. & Rost, T. L. Apical organization and maturation of the cortex and vascular cylinder in Arabidopsis thaliana (Brassicaceae) roots. Am. J. Bot. 89, 908–920 (2002)

    Article  Google Scholar 

  11. 11

    Imlau, A., Truernit, E. & Sauer, N. Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11, 309–322 (1999)

    CAS  Article  Google Scholar 

  12. 12

    Torres-Ruiz, R. A. & Jurgens, G. Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120, 2967–2978 (1994)

    CAS  PubMed  Google Scholar 

  13. 13

    Scheres, B. et al. Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121, 53–62 (1995)

    CAS  Google Scholar 

  14. 14

    Rubio, V. et al. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 15, 2122–2133 (2001)

    CAS  Article  Google Scholar 

  15. 15

    Scheres, B. et al. Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120, 2475–2487 (1994)

    CAS  Google Scholar 

  16. 16

    Di Laurenzio, L. et al. The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86, 423–433 (1996)

    CAS  Article  Google Scholar 

  17. 17

    Helariutta, Y. et al. SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101, 555–567 (2000)

    CAS  Article  Google Scholar 

  18. 18

    Lin, Y. & Schiefelbein, J. Embryonic control of epidermal cell patterning in the root and hypocotyl of Arabidopsis. Development 128, 3697–3705 (2001)

    CAS  PubMed  Google Scholar 

  19. 19

    Inoue, T. et al. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409, 1060–1063 (2001)

    ADS  CAS  Article  Google Scholar 

  20. 20

    Suzuki, T. et al. The Arabidopsis sensor His-kinase, AHK4, can respond to cytokinins. Plant Cell Physiol. 42, 107–113 (2001)

    CAS  Article  Google Scholar 

  21. 21

    Lawson, N. D. et al. Notch signaling is required for arterial–venous differentiation during embryonic vascular development. Development 128, 3675–3683 (2001)

    CAS  PubMed  Google Scholar 

  22. 22

    Lawson, N. D. & Weinstein, B. M. Arteries and veins: making a difference with zebrafish. Nature Rev. Genet. 3, 674–682 (2002)

    CAS  Article  Google Scholar 

  23. 23

    Yoshimura, T., Demura, T., Igarashi, M. & Fukuda, H. Differential expression of three genes for different β-tubulin isotypes during the initial culture of Zinnia mesophyll cells that divide and differentiate into tracheary elements. Plant Cell Physiol. 37, 1167–1176 (1996)

    CAS  Article  Google Scholar 

  24. 24

    McCann, M. Tracheary element formation: building up to a dead end. Trends Plant Sci. 2, 333–338 (1997)

    Article  Google Scholar 

  25. 25

    Wisman, E., Cardon, G. H., Fransz, P. & Saedler, H. The behaviour of the autonomous maize transposable element En/Spm in Arabidopsis thaliana allows efficient mutagenesis. Plant Mol. Biol. 37, 989–999 (1998)

    CAS  Article  Google Scholar 

  26. 26

    Liu, Y. G. et al. Complementation of plant mutants with large genomic DNA fragments by a transformation-competent artificial chromosome vector accelerates positional cloning. Proc. Natl Acad. Sci. USA 96, 6535–6540 (1999)

    ADS  CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank M. Kivimäki, K. Kainulainen, A. Hakonen, J. Immanen, Q. Yu, F. D. Rodriguez, G. Resch and M. Ilijin-Jug for technical assistance and plant cultivation; E. Jokitalo for TEM; M. Laxell and S. Tähtiharju for material; I. Bancroft and K. van de Sande at GARNet/GeTCID; N. Sauer for the AtSUC2::GFP line; E. Mellerowicz, F. Rook and M. Saarma for advice; and P. N. Benfey, B. Scheres and C. Alonso Blanco for comments on the manuscript. Financial support was provided by the Academy of Finland, Tekes, EU, EMBO and the University of Helsinki.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ykä Helariutta.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bonke, M., Thitamadee, S., Mähönen, A. et al. APL regulates vascular tissue identity in Arabidopsis. Nature 426, 181–186 (2003). https://doi.org/10.1038/nature02100

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing