Download View Full PDF - Biochemical Society Transactions

Intercellular Signalling in Plants
Reprogramming of root epidermal cells in
response to nutrient deficiency
P. Perry*, B. Linke† and W. Schmidt*1
*Institute of Plant and Microbial Biology, Academia Sinica, 115 Taipei, Taiwan, and †Department of Biology, Humboldt University, D-10115 Berlin, Germany
Abstract
Post-embryonic development of the root system is highly plastic to environmental cues, compensating for
the sessile lifestyle of plants. The fate of epidermal cells of Arabidopsis roots is particularly responsive to
nutritional signals, leading to an increase in the root’s surface area in the absence of the essential but immobile minerals iron, phosphate and manganese. The resulting phenotype is characteristic of the respective
condition. Growth under nutrient starvation affects the expression of genes involved in cell specification,
indicating that environmental signals are perceived at an early stage of cell development. Cell fate decisions
are controlled at different levels, probably integrated at the level of chromatin organization.
Form follows function
Roots provide the plant with water and nutrients, the supply
of which varies both temporarily and spatially. To optimize
soil exploration, plant roots show high plasticity, which is
conferred by changes in cell fate acquisition during post-embryonic development. Environmental signals can be superimposed on or integrated with endogenous developmental
programmes to best suit the changing edaphic conditions
encountered in their natural habitat. Plasticity is most apparent in the root epidermis, the tissue that is in direct contact
with the rhizosphere and is, thus, first affected by signals
derived from the immediate vicinity of the roots. Both the
frequency and the peculiarities of root hairs can change in
response to environmental cues, allowing for an improved
exploration of the soil.
A binary code in cell specification
Root epidermal cells can enter one of two developmental
pathways; they can differentiate as a root hair cell or become a
non-hair cell. Decisions to enter either cell fate are determined
by positional information. Cells that are in contact with two
underlying cortical cells develop into a hair cell, while those
that lie over a periclinal cortical cell wall differentiate as a
non-hair cell [1]. The positional information is conveyed by
a recently identified receptor-like protein kinase named SCM
(SCRAMBLED) [2]. SCM targets a set of transcription factors genes that, in complex interaction including cell-to-cell
movement between non-hair cells and hairs cells, define the
specification of the cell [3,4]. A central role in both the hair
and non-hair cell fate is played by the Myb-type transcription
factor WER (WEREWOLF) which, in non-hair cells, forms
a complex with the R-like bHLH (basic helix–loop–helix)
proteins GL3 and EGL3 and the WD40 protein TTG
Key words: cell fate, cell specification, epidermal cell, nutrient deficiency, plant development,
plasticity, root hair.
Abbreviations used: SCM, SCRAMBLED; TTG, TRANSPARENT TESTA GLABRA; WER, WEREWOLF.
1
To whom correspondence should be addressed (email [email protected]).
(TRANSPARENT TESTA GLABRA). The WER–GL3–
EGL3–TTG complex promotes the expression of the singlerepeat Myb protein CPC and of the homeodomain leucine
zipper protein GL2. GL2 acts as a positive regulator of the
non-hair cell fate. In hair cells, the expression of WER is
repressed by SCM. CPC moves from non-hair cells into
hair cells, suppressing the binding of WER to the GL3–TTG
complex and a new complex composed of CPC–GL3–EGL3
and TTG is formed that blocks the expression of CPC and
GL2 in future hair cells.
Different paths to one goal
The fate of epidermis cells is not irreversibly fixed but reached
by continuous integration of different signals. In mature
roots, the root hair number is significantly reduced compared
with seedlings. Only three out of the eight cells in the hair
position enter the hair cell fate [5]. In addition, the epidermal patterning becomes responsive to the environment.
Length, frequency and position of the hairs are particularly
affected by the availability of sparingly soluble nutrients such
as phosphate (P), iron (Fe) and manganese (Mn), in a manner
typical of each growth type (Figure 1). P-deficient plants
develop hairs that are approx. 3-fold longer than those of control plants. The frequency of hairs is almost doubled, which
is due to an increased number of epidermal cells developing into hairs both in the normal location and in positions
normally occupied by non-hair cells. Such ectopic hairs
are rarely found under control or Fe-deficient conditions.
In response to Fe deficiency, an increase in surface area is
achieved by forming hairs with bifurcated tips. Approximately half of the hairs of Fe-deficient plants are branched,
leading to a substantial increase in exposed surface of the
plasma membrane without a significant increase in the number of cells forming root hairs [5]. The Fe stress phenotype
is installed after a ‘silent phase’ in which no root hairs are
formed, indicating a reorganization of the epidermal pattern
after the signal has been received. Mn deficiency induces both
C 2007
Biochemical Society
161
162
Biochemical Society Transactions (2007) Volume 35, part 1
Figure 1 Modifications of root epidermal cells by nutrient deficiency
(A) Control, (B) Fe deficiency, (C) P deficiency and (D) Mn deficiency. Scale bar, 50 µm. Note the formation of bifurcated
hairs in (B, D).
strategies, but the overall number of root hairs is intermediate
between the Fe- and P-deficient growth types.
Multiple levels of regulation
A survey of mutants defective at various stages of root
hair development revealed that divergence in root epidermal
patterning was most pronounced in mutants defective in
auxin and ethylene signalling and in those harbouring defects
in cell specification [5,6]. A distinct set of genes appears to
be required for inducing the phenotype that is characteristic
of the nutritional status of the plant. This set of genes differs
among the position of the epidermal cell (hair versus non-hair
position), indicating that the positional signal is necessary for
inducing the respective root hair pattern.
Changes in root epidermal patterning are associated with
differential expression of cell specification genes, providing
evidence that environmental signals are perceived at an early
stage of cell differentiation. In particular, genes determining
the non-hair cell fate such as WER and GL2 are down-regulated in response to nutrient deficiency, resulting in a more
‘relaxed’ state of the epidermis, allowing more cells to develop
C 2007
Biochemical Society
into hair cells (B. Linke, W. Schmidt and T.J. Buckhout,
unpublished work).
Both the downstream targets of the cell specification genes
and the upstream events leading to their altered expression are
unknown. An attractive model is the integration of different
signals at the level of chromatin organization. Mutants defective in chromatin assembly such as fas2 show impaired epidermal patterning. Positional information depends on the chromatin state of the root hair repressor gene GL2. The
chromatin state around the GL2 locus is subject to positional
information and reorganized when epidermal cells divide
and change its position relative to the underlying cortical
cells [7]. Changes in histone acetylation alter the expression
of key players in epidermal cell specification, providing
evidence for a central role of chromatin remodelling in
epidermal cell patterning [8]. Alternative states of chromatin
organization around the GL2 locus provide a possibility of
switching epidermal cell fate in response to environmental
information.
Genetic and pharmacological studies revealed that the
development of branched hairs in response to Fe deficiency
is inhibited both by auxin and ethylene antagonists as well
Intercellular Signalling in Plants
as in mutants defective in auxin or ethylene signalling [9]. In
contrast, no requirement for functional auxin and ethylene
signalling cascades was apparent from these studies for the
formation of extra root hairs in P-deficient roots [9]. Striking
examples are the auxin-transport mutants trh1 and the auxin
signalling mutant axr2, which do not form root hairs under
control and Fe-deficient conditions, but form normal hairs
under P-deficient conditions.
Besides local availability of nutrients, the fate of root
epidermal cells is affected by remote signals from the shoot.
The mechanisms underlying shoot control of root development and the nature of internal long-range signals have not
yet been identified. Proteins and RNA molecules are putative
candidates intersecting with cell local sensing of nutrients.
Long-range movement via the phloem has been shown
for proteins as well as for RNA [10]. The phloem sap contains both siRNA (small interfering RNA) and miRNA
(microRNA) species, supporting a potential involvement of
small RNAs in the control of developmental plasticity [11].
Destination-selective trafficking of phloem proteins has been
demonstrated, indicating that, similar to the intercellular
transport of transcription factors, long-distance transport of
macromolecules can be actively controlled [12].
References
1 Dolan, L. (2006) J. Exp. Bot. 57, 51–54
2 Kwak, S.H., Shen, R. and Schiefelbein, J. (2005) Science 307, 1111–1113
3 Bernhardt, C., Zhao, M., Gonzalez, A., Lloyd, A. and Schiefelbein, J. (2005)
Development 132, 291–298
4 Koshino-Kimura, Y., Wada, T., Tachibana, T., Tsugeki, R., Ishiguro, W. and
Okada, K. (2005) Plant Cell Physiol. 46, 817–826
5 Müller, M. and Schmidt, W. (2004) Plant Physiol. 134, 409–419
6 Schikora, A. and Schmidt, W. (2001) Protoplasma 218, 67–75
7 Costa, S. and Shaw, P. (2006) Nature 439, 493–496
8 Xu, C.R., Liu, C., Wang, Y.L., Li, L.C., Chen, W.Q., Xu, Z.H. and Bai, S.N.
(2005) Proc. Natl. Acad. Sci. U.S.A. 102, 14469–14474
9 Schmidt, W. and Schikora, A. (2001) Plant Physiol. 125, 2078–2084
10 Lough, T.J. and Lucas, W.J. (2006) Annu. Rev. Plant Biol. 57, 203–232
11 Yoo, B.C., Kragler, F., Varkonyi-Gasic, E., Haywood, V., Archer-Evans, S.,
Lee, Y.M., Tony, J., Lough, T.J., William, J. and Lucas, W.J. (2004) Plant Cell
16, 1979–2000
12 Aoki, K., Suzui, N., Fujimaki, S., Dohmae, N., Yonekura-Sakakibara, K.,
Fujiwara, T., Hayashi, H., Yamaya, T. and Sakakibara, H. (2005) Plant Cell
17, 1801–1814
Received 25 August 2006
C 2007
Biochemical Society
163