REVIEWS SIGNALS THAT CONTROL PLANT VASCULAR CELL DIFFERENTIATION Hiroo Fukuda 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. PLANT CELL BIOLOGY VASCULAR CELLS The body plan of plants is controlled by a combination such as PROCAMBIUM and VASCULAR CAMBIUM.But MONO- Cells that form the plant of clonal fate and positional information that is pro- COTYLEDONOUS PLANTS and ferns, in which secondary vascular tissues, including vided by local signals, as is commonly seen in multicel- thickening growth does not occur, lack cambium. procambial cells, cambial cells, lular organisms. Recent advances in molecular genetics Individual species of vascular plants form distinct radial sieve elements, companion cells, fibre cells, xylem and phloem and genome biology have uncovered unique mecha- patterns of vascular bundles in each organ, which have parenchyma cells, and tracheary nisms of plant-body formation. Vascular cells are been categorized as collateral, bicollateral, amphivasal elements. formed under a well-defined plant-differentiation pro- or amphicribral patterns (FIG. 1a, b). gramme. Although vascular cells usually differentiate at Procambial cells are vascular stem cells that are APICAL MERISTEM predicted positions and at a predicted time to form a derived from the apical meristem and give rise to xylem The meristematic tissue that is located at the tip of the shoot specific vascular pattern, the arrangement of the vascular and phloem precursor cells. The final step in vascular and root. It is composed of stem network can be altered by local signals or in response to development is the specification into distinct types of cells, which allow plants to environmental stimuli. This indicates the involvement vascular cells from the precursor cells. Phloem precur- continue to grow in height. of a non-clonal and flexible mechanism in vascular-pat- sor cells differentiate into various phloem cells such as SIEVE ELEMENTS SIEVE TUBES XYLEM tern formation. (which are components of ), The tissue that is responsible for VASCULAR CELLS are produced continuously from the COMPANION CELLS,phloem PARENCHYMA cells and phloem transporting water and APICAL MERISTEMS of shoots and roots in adult plants (FIG. 1). fibres. Xylem precursor cells give rise to TRACHEARY minerals. It also gives strength to In this situation, local cell–cell communication between ELEMENTS (TEs), xylem parenchyma cells and xylem the stem. developing vascular cells and cells that are not destined fibres, which together form xylem. TEs are components PHLOEM to differentiate into vascular cells might have a pivotal of a vessel — or tracheid — and at maturity, they are The tissue that is responsible for role in determining vascular cell differentiation. On the emptied by the loss of all cell contents, including the transporting the carbohydrates other hand, long-distance signalling also seems to be nucleus, to form hollow tubes through which fluids that are produced in leaves. necessary for the continuous production of vascular move. Therefore, cell death of TEs is programmed strands. developmentally. TEs possess a characteristic secondary Department of Biological Vascular strands connect plant organs that are often cell wall of annular, spiral, reticulate or pitted wall thick- Sciences, Graduate School separated by many metres, and provide a pathway for enings, which add strength and rigidity to the wall and of Science, The University the transport of signalling molecules as well as water prevent TEs from collapse under the high pressure that of Tokyo, 7-3-1 Hongo, and nutrients. For such vascular function, their conti- is exerted on fluid uptake. Tokyo 113-0033, Japan. nuity is a prerequisite.Vascular strands — which are Molecular-genetic studies with Arabidopsis thaliana e-mail: [email protected]. u-tokyo.ac.jp also referred to as vascular bundles — are composed of mutants and cellular studies with Zinnia elegans xylo- doi:10.1038/nrm1364 three tissues: XYLEM, PHLOEM and meristematic tissues genic cultures (BOX 1) have revealed the integrated NATURE REVIEWS | MOLECULAR CELL BIOLOGY VOLUME 5 | MAY 2004 | 379 © 2004 Nature Publishing Group REVIEWS Xylem a TE parenchyma c PROCAMBIUM A primary meristem that is derived from the apical Ph Pr Xy meristem and which gives rise to b primary vascular tissues and vascular cambium. Ph Xy VASCULAR CAMBIUM A lateral meristem that gives rise Collateral Bicollateral Amphicribral Amphivasal to secondary vascular tissues — d 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 Figure 1 | Vascular-pattern formation. a | The vascular system is composed of phloem (green, Ph), procambium (and/or vascular other by sieve plates. In contrast cambium; yellow, Pr) and xylem (Xy) that contains tracheary elements (grey) and xylem parenchyma cells (red), which make a distinct to tracheary elements, which are radial pattern of vascular bundles depending on the organ and plant species. Reproduced with permission from © (1982) depleted of all cell contents, sieve REF.120 elements contain a nucleus even John Wiley & Sons Inc. b | Four distinct radial patterns of phloem and xylem (red) within vascular bundles. c | The procambium, after maturation. stained blue to show the promoter activity of the HD-ZIP-III homeobox gene AtHB8, is formed as continuous columns of cells in embryos. In seedlings, the shoot and root meristems produce procambial cells to keep the continuity of vascular bundles. SIEVE TUBE Reproduced with permission from REF.119 © (2000) Shujyunsha Co. Ltd. d | van3 mutants have a fragmented vascular network 14 A series of sieve elements that in a cotyledon (right) compared with that in a wild-type cotyledon (left) . Reproduced with permission from REF.14 © (2000) form a long cellular tube The Company of Biologists Ltd. that functions in the transport of photosynthetic products. COMPANION CELLS Cells that are associated with nature of plant vascular formation, including the and controlling factor in the regeneration of vascular sieve elements and support integrity of the vascular system, intravascular-radial- strands around a wound. These studies also showed that them. An asymmetrical 1,2 cell division of a precursor cell pattern formation and vascular cell specification . polar auxin flow is needed for continuous vascular- produces a sieve element and a Here,I review recent findings on plant vascular cell dif- pattern formation. Indeed, the prevention of polar companion cell. ferentiation, with a special emphasis on intercellular and auxin transport by specific inhibitors causes the forma- intracellular signalling. Because little is known about the tion of local aggregates of vascular cells and discontinu- PARENCHYMA molecular mechanism of phloem cell differentiation, ous veins in newly developed leaves6,7.By contrast, such A tissue that is composed of cells that have thin cell walls and has a vascular cell differentiation is described mainly with inhibitors were less effective at inhibiting vascular differ- relatively flexible ability to regard to xylem cell differentiation. In appropriate cases, entiation from the procambium, patterns of which had differentiate. A. thaliana and Z. elegans genes and proteins are distin- already formed in embryonic cotyledons. So, these guished by the prefixes At and Ze, respectively. inhibitors seem to affect vascular development through TRACHEARY ELEMENT The thick-walled cylindrical cell disruptions in the development of procambial patterns. 4,5 that is a component of vessels, or Intercellular signals and vascular continuity Sachs proposed the ‘auxin-flow canalization hypothe- tracheids, which are water- A role for auxin flow. Pioneering studies by Jacobs3 and sis’,which suggests that auxin flow, starting initially by conducting tissues. Sachs4,5 showed that indoleacetic acid (IAA) — a nat- diffusion, induces the formation of the polar-auxin- ural auxin that is produced in the apical region of transport-cell system.This, in turn, promotes auxin BASIPETALLY Toward the root tip from the shoots (including the apical meristem and expanding transport, leading to canalization of the auxin flow shoot tip. leaves) and transported BASIPETALLY — was the limiting along a narrow column of cells (FIG. 2).This continuous 380 | MAY 2004 | VOLUME 5 www.nature.com/reviews/molcellbio © 2004 Nature Publishing Group REVIEWS Box 1 | Xylem cell differentiation induced in vitro without cell division Single mesophyll cells (see figure part a,left panel) can be a isolated mechanically from expanding leaves of Zinnia elegans.When the isolated mesophyll cells are cultured in vitro in the presence of auxin and cytokinin, they transdifferentiate synchronously within 72 hours, and at a high frequency, into tracheary