Аннотация:POSITIONAL CONTROL
OF PLANT TISSUE DIFFERENTIATION
Vladimir V. Choob
Lomonosov Moscow State University, Moscow, Russia
choob_v@mail.ru
Plant tissue differentiation in ontogeny follows precise spatial patterns. The
procambial strand position is tightly associated with subsequent leaf and stem venation. Vascular bundles exhibit their polarity by formation of phloem and xylem
in the proper spatial and temporal mode. Leaf trichomes and guard cells display
visible proximal order with prohibition of new trichome or stomata formation in
close neighborhood to each other. All these examples demonstrate that plant cells
should differentiate according to various positional signals, emitting by singular
cells or cell groups.
The term of positional information was invented by Lewis Wolpert (1969),
who was attempted to solve the problem of differentiation of identical cells in
concordance with their position. His famous model of French flag postulates the
existence of some source of positional signal (morphogen). The morphogen concentration should decrease as it diffuses through the field of cells. Several threshold
levels of morphogen concentration define the developmental fate of every cell, thus
depending on the positional signal.
Differentiation of phloem and xylem from procambial strand could be wellcircumscribed by the French flag model. The cells of the presumptive protophloem excrete a small peptide of CLE-family (TDIF), which plays the role of the
positional signal. The concentration of TDIF decreases with the distance from
the protophloem pole. Non-differentiated procambial cells expose the membrane
receptor PXY, specifically binding to CLE-peptide (Fisher, Turner, 2007). The
high level of CLE-peptide TDIF causes phloem differentiation, medium level of
TDIF leads to cambial cell formation, whereas low level / absence of TDIF induces xylem development (Etchells, Turner, 2010). Thus mutations in TDIF or
PXY drive toward xylem overproduction and defects in phloem differentiation,
while the hyper-expression of TDIF has the opposite effect of massive phloem
development.
Extracellular position signals in the form of small cysteine-rich peptides
are used in stomata patterning. In Arabidopsis the meristemoid cells synthesize
EPIDERMAL PATTERNING FACTORS 1 and 2 (EPF1, EPF2), inhibiting new
meristemoid formation in close proximity to the existing ones. As a consequence of
dysfunction of this positional signaling system, multiple clustered stomata develop
in mutants too many mouth, encoding the subunit of the membrane EPF-receptor
36
complex, whereas the EPF1/2 overproduction is accompanied in low stomata density (Zoulias et al., 2018).
Positional signals may be distributed within plant cells through plasmodesmata. The establishment of radial patterning in root requires the interplay
of central cylinder and cortical cell signals. In Arabidopsis, transcription factor SHORT ROOT (SHR) is transferred from pericycle cell lineage to the
presumptive endodermis, where it induces expression of transcription factor
SCARECROW (SCR). Mutual effect of SHR and SCR drives the cells to endodermal differentiation. Rapid cessation of positional signal toward cortex
parenchyma cells occur due to block of transfer from endodermal lineage to
cortex parenchyma via plasmodesmata (Helariutta et al., 2000). The mutation in
SCR gene causes complete loss of endodermis in roots and starch sheath layer
in shoots. These observations render the role of SCR in radial patterning both
in roots and shoots (Wysocka-Diller et al., 2000). Recently, the involvement of
SHR–SCR system of positional signaling, exploiting the same principles of plasmodesmatal transfer, was postulated for mesophyll–bundle sheath differentiation
during the establishment of Kranz-anatomy in C4
leaves (Slewinski et al., 2012;
Fouracre et al., 2014).
All the listed examples suggest the important role of positional information
in plant tissue differentiation, despite the diversity of the underlying molecular
mechanisms. Therefore, the positional signaling orchestrates the proper spatial
organization of plant tissues, necessary to fulfill their physiological functions.
References
Etchells J.P., Turner S.R. 2010. The PXY–CLE41 receptor ligand pair defines a multifunctional
pathway that controls the rate and orientation of vascular cell division. Development 137:
767–774.
Fisher K., Turner S.R. 2007. PXY, a receptor-like kinase essential for maintaining polarity during
plant vascular-tissue development. Curr. Biol. 17: 1061–1066.
Fouracre J.P., Ando S., Langdale J.A. 2014. Cracking the kranz enigma with systems biology. J. Exp.
Bot. 65: 3327–3339.
Helariutta Y., Fukaki H., Wysocka-Diller J., Nakajima K., Jung J., Sena G., Hauser M.T., Benfey
P.N. 2000. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through
radial signaling. Cell 101: 555–567.
Slewinski T.L., Anderson A.A., Zhang C., Turgeon R. 2012. Scarecrow plays a role in establishing
kranz anatomy in maize leaves. Plant Cell Physiol. 53: 2030–2037.
Wolpert L. 1969. Positional information and the spatial pattern of cellular differentiation. J. Theor.
Biol. 25: 1–47.
Wysocka-Diller J.W., Helariutta Y., Fukaki H., Malamy J.E., Benfey P.N. 2000. Molecular analysis
of SCARECROW function reveals a radial patterning mechanism common to root and shoot.
Development 127: 595–603.
Zoulias N., Harrison E.L., Casson S.A., Gray J.E. 2018. Molecular control of stomatal development.
Biochem. J. 475: 441–454.