Journal of Experimental Botany, Vol. 64, No. 17, pp. 5263–5268, 2013
doi:10.1093/jxb/ert248 Advance Access publication 23 August, 2013
review paper
GOLVEN peptides as important regulatory signalling
molecules of plant development
Ana Fernandez1,2,*, Pierre Hilson3,4 and Tom Beeckman1,2
1
Department of Plant Systems Biology, VIB, B-9052 Ghent, Belgium
Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Ghent, Belgium
3
INRA, UMR1318, Institut Jean-Pierre Bourgin, RD10, F-78000 Versailles, France
4
AgroParisTech, Institut Jean-Pierre Bourgin, RD10, F-78000 Versailles, France
2
* To whom correspondence should be addressed. E-mail: [email protected]
Received 30 May 2013; Revised 8 July 2013; Accepted 10 July 2013
Abstract
The contribution of signalling peptides to plant development is increasingly evident as more new peptide families become identified. The recently discovered GLV/RGF/CLEL secreted peptide family comprises 11 members in
Arabidopsis and has been shown by independent research groups to be involved in different plant developmental
programmes such as root meristem maintenance, root hair development, and root and hypocotyl gravitropism. This
short review summarizes our current knowledge on GLV/RGF/CLEL peptides and highlights future challenges to decipher their function.
Key words: CLE-like (CLEL), GOLVEN (GLV), peptide signalling, root meristem growth factors (RGFs).
Introduction
In recent years, multiple genes coding for small secreted peptides have been discovered that control various aspects of
plant development (Murphy et al., 2012). Among them, the
GOLVEN (GLV)/root meristem growth factor (RGF)/CLElike (CLEL) gene family has been described by three independent groups (Matsuzaki et al., 2010; Meng et al., 2012;
Whitford et al., 2012), thereby explaining the redundant
nomenclature (Table 1). For clarity, they will be referred to as
the GLV genes and gene products hereafter. This short review
summarizes the results published so far describing the role of
the GLV peptides.
Structure of GLV peptides
GLV genes were originally identified in Arabidopsis thaliana,
but are conserved throughout the plant kingdom (Whitford
et al., 2012). They code for small post-translationally modified peptides. Experimental evidence and similarity to other
secreted signalling peptides suggest that the mature bioactive
GLV peptides are produced by proteolytic cleavage of larger
precursor proteins that share a common structure (Matsuzaki
et al., 2010; Meng et al., 2012; Whitford et al., 2012). The
GLV predicted precursor proteins have a length of 86–163
amino acids. Two main domains can be distinguished in their
primary sequence (Fig. 1). The N-terminal domain contains
a signal peptide (SP) that targets the protein to the secretory
pathway. The C-terminal domain contains a motif conserved
among all GLV members that defines the family and codes
for the functional secreted mature peptide. A third region
with little sequence similarity between GLV pre-proproteins
connects the two aforementioned domains (Matsuzaki et al.,
2010; Meng et al., 2012; Whitford et al., 2012).
The genes coding for the GLV/RGF/CLEL peptides were
identified in three independent in silico studies (Matsuzaki
et al., 2010; Meng et al., 2012; Whitford et al., 2012). Because
the sequence homology parameters differed between them,
some genes were not originally identified by all three groups
© The Author 2013. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved.
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5264 | Fernandez et al.
Table 1. Summary of the nomenclature of GLV/RGF/CLEL genes
AGI code
Whitford
et al. (2012)
Matsuzaki et al.
(2010)
Meng et al.
(2012)
At4g16515
At5g64770
At3g30350
At3g02240
At1g13620
At2g03830
At2g04025
At3g02242
At5g15725
At5g51451
At5g60810
AT1G66145
GLV1
GLV2
GLV3
GLV4
GLV5
GLV6
GLV7
GLV8
GLV9
GLV10
GLV11
–
RGF6
RGF9
RGF4
RGF7
RFG2
RGF8
RGF3
–
–
RGF5
RGF1
–
CLEL6
CLEL9
–
CLEL4
CLEL1
CLEL2
CLEL3
CLEL5
–
CLEL7
CLEL8
CLE18
(–) indicates that the gene was not retrieved in the corresponding study.
peptides corresponding to the GLV motif greatly increased
bioactivity, with phenotypes observed at nanomolar concentrations when applied to Arabidopsis seedlings (Matsuzaki
et al., 2010; Whitford et al., 2012). Hydroxyprolination has
been shown to increase the bioactivity of other plant peptides
and may be further modified with the addition of O-linked
l-arabinose chains (Matsubayashi, 2011). However the presence of hydroxyprolines in GLV mature peptides has not yet
been associated with any functional role.
GLV gene expression
Expression patterns have been reported for all Arabidopsis
GLV genes. They are collectively found in all parts of the
plant including the root and the shoot, and during the vegetative and reproductive stages. Nevertheless the expression of
different GLV genes is confined to specific cells or cell types.
Root
Fig. 1. The structure of GLV precursor proteins consists of two
conserved domains connected by a variable region. The sequence
of the native peptides has been identified for GLV1, 2, 3, and 11.
(SO3) indicates a sulphated tyrosine residue, and (Hyp) refers to a
hydroxyproline residue. SP, signal peptide; GLV, GLV motif.
(Table 1). The current consensus is that the GLV/RGF/CLEL
family comprises 11 members in Arabidopsis, all sharing the
tripartite pre-proprotein structure described above. One additional pre-propeptide previously classified in the CLV3/ESR
(CLE) peptide family, CLE18, has been linked to GLV peptides (Meng et al., 2012). However, unlike the other GLV/RGF/
CLEL precursors that carry a single conserved motif at or
near their C-terminal side, the peculiar CLE18 pre-proprotein
contains two such motifs: the first is embedded in the variable
region and is reminiscent of the CLE peptide motif; and the second is positioned at the C-terminal end of the precursor and is
similar to the GLV motif. Since the CLE18 GLV motif was the
input sequence for Meng et al. (2012) to search for homologues
and because most CLE and GLV precursors share a similar
domain structure, they were named CLE-like (CLEL) peptides
in this report. So far, the functional implication of the presence
of these two different motifs in the same protein is unclear.
The sequence of the native secreted peptide has been determined for GLV1, GLV2, GLV3, and GLV11 (Fig. 1). They are
respectively 14, 15, 18, and 13 amino acids in length (Matsuzaki
et al., 2010; Whitford et al., 2012) and carry two types of
post-translational modifications: tyrosine sulphation and
hydroxylation of one of the proline residues. As for secreted
peptides of other families, tyrosine sulphation of synthetic
Expression analysis in promoter–reporter lines, together
with qRT–PCR studies, revealed that nine of the 11 GLV
genes are active within the primary root and can be classified in three groups (Fernandez et al., 2013) (Fig. 2A). The
first group comprises genes expressed in the quiescent centre
(QC) and/or columella cells: GLV5, GLV6, GLV7, GLV10,
and GLV11. The second group includes genes active in the
meristematic region above the QC, mainly in the endodermis
and cortex, but also in some vascular and epidermal cells:
GLV3, GLV6, and GLV9. The third group corresponds to the
genes transcribed in regions of the root above the meristem:
GLV4 in the epidermis and GLV8 in the epidermis and cortex. The transcription of GLV5, GLV7, and GLV11 has also
been mapped by in situ hybridization, in agreement with the
reporter line results (Matsuzaki et al., 2010). No expression
for GLV1 or GLV2 has been reported in the main root.
In addition, expression of 10 GLV genes was detected in
lateral roots (LRs) of the corresponding promoter–reporter
lines (Fig. 2B). Interestingly, GLV promoter activity is activated at different stages of primordium or LR development.
GLV6, GLV5, GLV10, GLV7, and GLV11 (in order of promoter induction) are transcribed early during primordium
formation (from stage I to IV, according to Malamy and
Benfey, 1997). GLV3 expression starts at primordium stage
V and that of GLV9 and GLV2 after emergence. GLV4 and
GLV8 are only transcribed in mature LRs, with transcription
patterns similar to those found in the main root.
To summarize, most GLV genes are active in specific portions of the root, suggesting they take part in different developmental processes. We recently proposed, as elaborated
on below, that the three GLV expression domains observed
within the primary root correspond to three functional
groups (Fernandez et al., 2013).
Shoot
GLV gene expression is not only restricted to the root,
and has also been reported in shoot tissues including the
GOLVEN peptides in plant development | 5265
Fig. 2. (A) Summary of GLV expression patterns and functions reported so far. (B) GLV transcript appearance during primordium and
lateral root (LR) development. Corresponding GLV overexpression phenotypes are indicated underneath. Primordium stages I–IV are
shown according to Malamy and Benfey (1997). E, emerged; ELR, emerged LR. Modified from Fernandez et al., 2013, Plant Physiology
161, 954–970 (Copyright American Society of Plant Biologists; www.plantphysiol.org).
hypocotyl, shoot apical meristem (SAM), cotyledon, leaf,
stem, and flower (Fernandez et al., 2013). As observed
in the root, GLV genes display differential expression in
shoot organs, often confined to specific cell types or tissues. While sometimes partially overlapping, GLV shoot
patterns are mostly specific to each gene. In young seedlings, GLV1, GLV2, GLV6, and GLV8 expression displays
different patterns in cotyledons and leaves, while GLV6 is
also found in the SAM and GLV8 in the stipules. Similarly,
GLV1, GLV2, GLV6, and GLV8 are expressed in different floral organs, whereas GLV7 was detected only in the
pollen (Fig. 2A). Although so far no clear functions for
GLV genes have been ascribed to distinct developmental
processes in the shoot, their cell- and tissue-specific expression patterns suggest a potential involvement in the aboveground parts.
Developmental programmes involving GLV
peptide signals
Root gravitropism
Overexpression of GLV genes results in a striking wavy
and curly root phenotype that is further enhanced when
the seedlings are germinated on slanted plates. Referring to
this phenotype, they were named GOLVEN (GLV) which
means ‘waves’ in Dutch (Whitford et al., 2012). Systematic
overexpression of all GLV genes showed that up-regulation
of GLV3, GLV6, and GLV9 resulted in the strongest curly
root phenotype (Fernandez et al., 2013). This is an interesting observation because these three genes are transcribed
in a similar domain above the QC within the primary root
meristem (Fig. 2A). Quantitative gravistimulation assays
with GLV3 gain- and loss-of-function lines, consisting of the
5266 | Fernandez et al.
rotation of vertically grown seedlings by a 90 ° angle, revealed
that the root response to gravistimulation was affected when
GLV3 levels were altered: GLV3 overexpression results in
partially agravitropic roots, while the gravitropic response
of amiRglv3 seedlings was enhanced. Addition of synthetic
GLV3 peptide to the growth medium under the same conditions also resulted in altered gravitropic responses (Whitford
et al., 2012). Similarly, treatment with other GLV peptides
disturbed the root growth direction of Arabidopsis seedlings grown on slanted plates (Fernandez et al., 2013). These
results indicate that GLV peptides participate in the control of root gravitropic responses and that the level of GLV
signal(s) in the root tip must be precisely tuned for normal
gravitropic growth. It is likely that GLV peptides encoded by
distinct genes act redundantly in this process because roots
overexpressing different GLV family members or treated with
different synthetic peptides displayed similar phenotypes,
and because lines silenced solely for GLV3 showed only mild
defects in gravitropism.
The phenotype observed in GLV gain-of-function roots
is reminiscent of mutants affected in the transport or the
response to the phytohormone auxin. Therefore, we investigated whether GLV peptide and auxin pathways converge
to control gravitropic responses, and discovered that GLV
peptides modulate auxin fluxes following gravistimulation
(Whitford et al., 2012). Treatment with GLV peptides hampers
the formation of the lateral auxin gradient in gravistimulated
roots. This gradient depends on the differential turnover of the
auxin efflux carrier PIN2 between the lower and upper side
of gravistimulated roots. Analysis of the PIN2 protein distribution in the plasma membrane (PM) of root tip epidermal
cells showed that the PIN2 differential was reduced in GLV3
gain- and loss-of function mutants or upon peptide treatment.
In addition, immunolocalization studies revealed that PIN2
protein levels in the PM of meristematic cells correlated with
GLV3 transcript levels; that is, the PIN2 level was higher and
lower in lines where GLV3 was overexpressed and silenced,
respectively. Furthermore, GLV3 peptide addition resulted in
the rapid accumulation of PIN2 in the PM and intracellular
vesicles. In summary, the GLV3 peptide—probably with GLV6
and GLV9—appears to be secreted from inner cells layers
(endodermis and cortex) in the root apical meristem (RAM)
and modulates PIN2 intracellular trafficking in outer tissues,
thereby altering the formation or maintenance of auxin gradients in the course of gravitropic responses. The molecular
mechanism explaining how the extracellular GLV signal is perceived and relayed to control PIN2 trafficking is still unknown.
Root apical meristem homeostasis
The GLV/RGF peptide family was identified by Matsuzaki
et al. (2010) because a sulphated 13 amino acid synthetic peptide derived from the C-terminal end of the GLV11/RGF1
precursor partially complements the short root phenotype of
tpst mutant plants. Tyrosylprotein sulphotransferase (TPST)
is apparently the sole enzyme catalysing tyrosine sulphation
in Arabidopsis, and the tpst loss-of-function mutant displays pleiotropic phenotypes, probably reflecting defects in
sulphated peptide signals (Komori et al., 2009; Zhou et al.,
2010). RGF1 peptide treatment specifically suppressed the
formation of extra QC cells observed in tpst roots and recovered meristematic activity in the presence of the additional
PSK and PSY1 sulphated peptides. They were therefore
named root meristem growth factors or RGFs. Although
single rgf1 (corresponding to GLV11), rgf2 (GLV5), and rgf3
(GLV7) mutants do not display root defects, the rgf1 rgf2 rgf3
triple mutant has a short-root phenotype characterized by a
decreased number of meristematic cortical cells. In agreement
with the complementation of the tpst mutant phenotype,
addition of the GLV11/RGF1 peptide to the rgf1 rgf2 rgf3
roots restored meristem size. Furthermore, overexpression of
all GLV genes in wild-type plants increases RAM size, albeit
to a different degree (Fernandez et al., 2013). These results
indicate that some GLV/RGF peptides are involved in the
control of meristematic activity in the primary root. However,
gene overexpression and peptide application resulted in variable effects on RAM activity depending on the GLV member
tested, suggesting that not all peptides have an endogenous
role in this process and that the observed effects may, in some
cases, be caused by the ectopic activation of non-cognate
signalling pathways. This may occur if related GLV peptide
ligands have residual affinity for their respective receptor(s),
as noted, for example, for CLV3/CLE signalling peptides
bound by the CLV1 membrane receptor (Ogawa et al., 2008).
The role of GLV/RGF peptides in meristem maintenance
involves the PLETHORA (PLT) transcription factors known
to control stem cell fate (Matsuzaki et al., 2010). The plt1
plt2 double loss-of-function mutant has a reduced response
to RGF1 peptide treatment, and addition of the RGF1 synthetic peptide modulates PLT gradients in the RAM, at both
the transcriptional and post-transcriptional levels. It has been
proposed that GLV/RGF peptides control meristem activity
mainly through stabilization of the PLT1 and 2 proteins.
Root hair development
Unlike the other GLV genes expressed in root tissues, GLV4
and GLV8 are transcribed above the RAM (Fig. 2A). The
GLV4 promoter is only active in the epidermal cells of the
root elongation zone and the beginning of the differentiation
zone. The GLV8 promoter drives gene expression in all the
cortical cells and the non-hair epidermal cells of the mature
root (Fernandez et al., 2013). This peculiar pattern suggested
that the corresponding peptides may be involved in root
developmental processes other than those described above.
This hypothesis was confirmed by the observation that certain GLV overexpression lines produce defective root hairs
characterized by the presence of extra branches. In agreement
with their expression pattern, GLV4 and GLV8 overexpression resulted in the strongest root hair phenotype, and only
loss-of-function mutants for these two genes had shorter hairs
(Fernandez et al., 2013). Root epidermal cells are arranged in
alternating files distinguished by their ability to produce root
hairs or not. It is assumed that this pattern is the result of a
cell–cell communication system that specifies trichoblast cells
located adjacent to the intercellular space between underlying
GOLVEN peptides in plant development | 5267
cortical cells (Tominaga-Wada et al., 2011). Epidermal cells
are capable of responding to a cortical signal via the plasma
membrane receptor kinase SCRAMBLED. However, while
root hair length was reduced in the glv8-1 null mutant, the
epidermal cell fate was not altered. It is therefore unlikely
that the GLV4 and GLV8 ligands function to specify epidermal cell identity. Instead, their function in root hair development is probably only restricted to assist in proper root hair
elongation.
Lateral root development
Ten out of 11 GLV genes are expressed during primordium
or LR development (Fernandez et al., 2013). In addition,
overexpression of some GLV genes resulted in a ‘naked’ primary root with very few emerged LRs. Strikingly, the ectopic
expression of GLV genes transcribed at early stages of primordium initiation (stage I–IV) produced a strong reduction
in the LR number, while those transcribed at later stages had
only a minor effect (Fig. 2B). Treatments of wild-type plants
with some GLV synthetic peptides had a similar effect (Meng
et al., 2012). Although LR phenotypes in GLV loss-of-function mutants have not been analysed yet, expression data
together with overexpression phenotypes suggest that GLV
genes may also act during LR development.
Shoot development
While GLV1 and GLV2 are not transcribed in the main
root, they are found in the outer cell layers of Arabidopsis
hypocotyls (Whitford et al., 2012). Interestingly, the expression of these genes becomes asymmetric upon hypocotyl
gravistimulation, with higher expression at the lower side of
the reoriented organ. Auxin also accumulates in the lower
side of gravistimulated hypocotyls and, not surprisingly,
auxin induces GLV1 and GLV2 transcription. Furthermore,
hypo­cotyls of GLV1 and GLV2 gain- and loss-of-function
mutants have impaired gravitropic responses. Therefore, by
analogy with GLV function in root gravitropism, GLV1 and
GLV2 peptides may also control the intracellular trafficking of PIN proteins that redirect auxin fluxes during hypo­
cotyl gravitropic responses (Rakusova et al., 2011). However,
the similarity between the root and hypocotyl reorientation
mechanisms remains to be investigated. The potential PIN
targets of the GLV signalling pathway have not yet been identified in the hypocotyl. Furthermore, in contrast to GLV1 and
GLV2 expression in the hypocotyl, no GLV gene has been
found to be asymmetrically transcribed in the root tip following its reorientation (unpublished results).
The expression of several GLV genes in other shoot
organs—including leaf, flower, and SAM domains—suggests
that they have additional roles in the aerial portion of the
plant. However, no phenotype has been reported so far to
substantiate this hypothesis. For example, it will be interesting to determine whether GLV genes and gene products modulate specific components of the auxin transport machinery
or key transcription factors in shoot cells as they do in the
root meristem.
Conclusions and future perspectives
The current data indicate that GLV peptides act in a similar
way to other described signalling peptides but their function
in plant development is different. Several lines of evidence
show that they are non-cell autonomous molecules that probably relay information to nearby cells. GLV bioactive peptides
have been detected in medium conditioned with GLV overexpression plants, indicating that they are secreted into the
apoplast. While the expression of some GLV genes has been
detected in the endodermis and cortical cells of the RAM,
they seem to control PIN2 protein trafficking in the epidermis. In addition, mutant phenotypes are often observed in
cells or tissues where gene transcription is not detected, for
example GLV8 is expressed in root cortical and non-hair cells
but glv8 mutants have shorter root hairs. Therefore, by analogy with other known signalling systems, secreted GLV peptides are likely to bind receptor proteins in adjacent cell layers
in which they trigger a signalling cascade. Nevertheless, it is
worth mentioning that a GLV-driven autocrine mechanism
cannot be excluded, for example in QC and RAM stem cells.
The results obtained by independent research groups demonstrate that GLV peptides regulate different processes of root
development. Yet, the dissection of the GLV signalling pathways has just begun and their discovery has prompted numerous questions that remain unanswered. For example, GLV
peptides are involved in the control of auxin fluxes within
the RAM on the one hand and in root meristematic activity
on the other hand. However, it is still unclear whether these
are the outputs of the same or different signalling pathways.
Importantly, the identification of the GLV receptor(s) and its
targets is essential and required to establish a molecular link
between GLV signalling, PIN trafficking, and PLT stability.
Based on the current data, it appears that GLV peptides
have multiple ways to interfere with root development. Both
meristem maintenance and gravitropism are processes heavily dependent on auxin. However, for gravitropic responses,
GLV peptides seem to act upstream, influencing auxin transport, whereas in the root stem cell niche they appear to act
downstream, on targets of the auxin signalling cascade.
Alternatively, GLV regulation of auxin fluxes may influence PLT gradients and thereby control meristem activity.
As another indication that GLV and auxin pathways may be
tightly interconnected, five GLV genes are transcriptionally
induced by auxin treatment (Zhou et al., 2010). In addition,
mutations in the gene encoding the TPST enzyme, catalysing
the sulphation of GLV peptides, affect the expression of PIN
genes and auxin biosynthetic genes, as well as auxin accumulation in the root tip. Similarly, peptides belonging to other
families have been shown to act in combination with phytohormone signalling (Chilley et al., 2006; Whitford et al., 2008;
Kondo et al., 2011; Kumpf et al., 2013). It is thus tempting to
speculate that the functions of locally secreted peptides and
phytohormone responses encode regulatory feedback loops
that determine the fate of specific cell populations in various
environments.
GLV expression and mutant phenotypes have been
described in different plant parts. Are these results pointing
5268 | Fernandez et al.
to shared signalling pathways? That is likely to be the case,
as for peptides belonging to the CLE and IDA/IDL families,
which are known to have similar functions in different plant
organs (Fletcher et al., 1999; Butenko et al., 2003; Stahl et al.,
2009; Kumpf et al., 2013). The regulation of auxin fluxes by
GLV peptides can explain their role in the differential cell
elongation resulting in gravitropic responses of root and
hypocotyls. They may also control root hair growth and LR
development through a similar mechanism, because auxin is
actively involved in both processes.
As for other families of secreted signalling peptides, some
of the basic knowledge necessary to understand GLV action
during plant development is still lacking. While the work
at hand is challenging, it is comforting to consider that the
coordinated development of the multicellular plant organs
involves a wide range of signalling molecules. The discovery
of the GLV/RGF/CLEL peptides added one tier to this complex phenomenon.
Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y. 2009.
Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proceedings
of the National Academy of Sciences, USA 106, 15067–15072.
Acknowledgements
Meng L, Buchanan BB, Feldman LJ, Luan S. 2012. CLE-like
(CLEL) peptides control the pattern of root growth and lateral root
development in Arabidopsis. Proceedings of the National Academy of
Sciences, USA 109, 1760–1765.
AF is supported by the Flemish Science Foundation (FWO
research project, G0273.13N). This work was in part financed
by grants of the Interuniversity Attraction Poles Programme
(IAP VI/33 and IUAP P7/29 ‘MARS’) from the Belgian
Federal Science Policy Office to TB, and the Integrated Project
AGRON-OMICS in the Sixth Framework Programme of the
European Commission (grant no. LSHG-CT-2006-037704)
to PH. We thank Dr Ive the Smet for useful comments on the
manuscript.
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