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Signals that control plant vascular cell differentiation

Nature Reviews Molecular Cell Biology volume 5, pages 379–391 (2004)Cite this article

Key Points

  • Asymmetrically transported auxin-efflux carriers cause a polarized flow of auxin, which leads to the formation of continuous columns of procambial cells. In addition, one or more auxin-flow-independent mechanisms might also be involved in the formation of the continuous columns.

  • Adaxial- and abaxial-identity genes might interact to specify xylem and phloem formation, respectively, to produce the intravascular radial pattern of vascular bundles of leaves.

  • Cytokinin has a crucial role in the formation and/or maintenance of procambial cells, probably together with auxin.

  • Brassinosteroids might initiate differentiation of procambial cells to xylem cells. This process might be associated with the positive and negative regulation of the expression of specific members of the HD-ZIP-III gene family by brassinosteroids and by the RNAi machinery, respectively.

  • Molecular and cellular studies with Zinnia elegans xylogenic cultures have uncovered details of a vascular-cell specification process — tracheary-element differentiation — during which coordinated gene expression is induced in association with patterned secondary-cell-wall formation and vacuole-executed programmed cell death.

Abstract

Plant vascular cells originate from procambial cells, which are vascular stem cells. Recent studies with Zinnia elegans cell culture and Arabidopsis thaliana mutants indicate that intercellular-signalling molecules such as auxin, cytokinin, brassinosteroids and xylogen regulate the maintenance or differentiation of procambial cells through distinct intracellular-signal transduction and gene-expression machineries. This intercellular- and intracellular-signalling system might be involved in determining the continuity and pattern formation of vascular tissues.

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Figure 1: Vascular-pattern formation.
Figure 2: Molecular mechanism of auxin polar transport.
Figure 3: Model for signalling processes in the maintenance and/or the differentiation of procambial cells and xylem cell precursors.
Figure 4: Radial-accumulation pattern of transcripts for homeobox genes in vascular tissues.
Figure 5: Programmed cell death during tracheary-element differentiation.

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Acknowledgements

The author thanks R. Jones, A. Jones, T. Berleth, J. Li, M. Sugiyama and J. Bowman for critical reading of the manuscript. This work was supported in part by Grants-in-Aid from the Ministry of Education, Science, Sports and Culture of Japan, from the Japan Society for the Promotion of Science and from the Mitsubishi Foundation.

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  1. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Tokyo, 113-0033, Japan

    Hiroo Fukuda

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  1. Hiroo Fukuda
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DATABASES

Interpro

START

TAIR

ARR15

AtHB8

AtHB15

AtPIN1

AUX1

auxin resistant-6

bodenlos

BRI1

BRL1

BRL2

cov1

GNOM

IAA8

MP

PHB

PHV

PINOID

REV

van3

wol

FURTHER INFORMATION

The Cellulose Synthase Superfamily

Glossary

VASCULAR CELLS

Cells that form the plant vascular tissues, including procambial cells, cambial cells, sieve elements, companion cells, fibre cells, xylem and phloem parenchyma cells, and tracheary elements.

APICAL MERISTEM

The meristematic tissue that is located at the tip of the shoot and root. It is composed of stem cells, which allow plants to continue to grow in height.

XYLEM

The tissue that is responsible for transporting water and minerals. It also gives strength to the stem.

PHLOEM

The tissue that is responsible for transporting the carbohydrates that are produced in leaves.

PROCAMBIUM

A primary meristem that is derived from the apical meristem and which gives rise to primary vascular tissues and vascular cambium.

VASCULAR CAMBIUM

A lateral meristem that gives rise to secondary vascular tissues — secondary xylem on the inner side and secondary phloem on the outer side in stems and roots, which results in an increase in the diameter of those organs.

MONOCOTYLEDONOUS PLANTS

A class of angiospermous plants that is characterized by the production of seeds with one cotyledon, such as rice, maize and wheat.

SIEVE ELEMENT

The components of sieve tubes that are separated from each other by sieve plates. In contrast to tracheary elements, which are depleted of all cell contents, sieve elements contain a nucleus even after maturation.

SIEVE TUBE

A series of sieve elements that form a long cellular tube that functions in the transport of photosynthetic products.

COMPANION CELLS

Cells that are associated with sieve elements and support them. An asymmetrical cell division of a precursor cell produces a sieve element and a companion cell.

PARENCHYMA

A tissue that is composed of cells that have thin cell walls and has a relatively flexible ability to differentiate.

TRACHEARY ELEMENT

The thick-walled cylindrical cell that is a component of vessels, or tracheids, which are water-conducting tissues.

BASIPETALLY

Toward the root tip from the shoot tip.

PROTOPHLOEM

The primary phloem that is first formed from procambium during organ development.

AUX/IAA PROTEINS

A class of short-lived nuclear proteins that share four conserved domains and that are generally encoded by early-auxin-response genes. They repress auxin responses by dimerizing with auxin-response factor (ARF) transcriptional activators that reside on auxin-responsive promoter elements.

MYB-LIKE TRANSCRIPTION FACTOR

A member of the transcription-factor family that contains the MYB motif, which consists of a helix-turn-helix structure with three regularly spaced Trp residues. This family is substantially larger in plants than in animals and functions in the regulation of a variety of events, including secondary metabolism and plant morphogenesis.

PETIOLE

The part of the leaf that connects the leaf blade and the stem.

CYTOKININ

N6-substituted adenine derivatives that have diverse effects on important physiological functions such as cell division, greening and differentiation in plants.

PERICYLCE

The tissue that is composed of one or a few layers of cells that are located outside of the vascular tissues in roots and stems. In roots, lateral roots originate from this tissue.

INTERFASCICULAR

'Between the bundles'; the bundles being the strands that contain the vascular tissue.

microRNA

The approximately 21–22-ribonucleotide RNA that arises from the action of the Dicer double-stranded ribonucleases on short stem-loop precursors. It initiates blocking of the targeted mRNAs, which have nucleotide sequences that are complementary to the microRNA.

BRASSINOSTEROID

A group of naturally occurring plant polyhydroxysteroids with wide-ranging biological activity.

MESOPHYLL

The photosynthetic tissue between the upper and lower epidermis of the leaf. Mesophyll cells contain chloroplasts.

ARABINOGALACTAN PROTEIN

A class of hydroxyproline-rich proteoglycans to which branched 3,6-β-D-galactans containing arabinose are attached by O-glycosidic bonds. They are widely distributed throughout the plant kingdom.

β-GLUCOSYL YARIV REAGENT

A synthetic phenyl glycoside that interacts selectively with arabinogalactan proteins and that is used for the purification and quantification of arabinogalactan proteins and for disturbing arabinogalactan protein function.

LIGNIFICATION

The deposition of lignin on secondary cell walls of tracheary elements and fibre cells to reinforce them mechanically and chemically.

LIM TRANSCRIPTION FACTOR

A member of the transcription-factor family that contains the LIM domain, which is a cysteine-rich polypeptide composed of two special zinc fingers separated by a two-amino-acid spacer.

MIDDLE LAMELLA

The thin layer that connects two plant cells and is rich in pectin.

TONOPLAST

The membrane that encompasses the central vacuole.

ENDOCARP CELL

The cell that composes the innermost fruit wall. Some endocarp cells are destined to die during maturation of the fruit.

ALEURONE CELL

The layered cell that surrounds the starchy endosperm of cereal grains and is instrumental in digesting the materials that are stored in the endosperm.

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Fukuda, H. Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5, 379–391 (2004). https://doi.org/10.1038/nrm1364

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