Sugars, Signalling, And Plant Development

Journal of Experimental Botany, Page 1 of 11doi:10.1093/jxb/err379

REVIEW PAPER

Sugars, signalling, and plant development

Andrea L. Eveland and David P. Jackson*

Cold Spring Harbor Laboratory, 1 Bungtown Rd, Cold Spring Harbor, NY 11724, USA

* To whom correspondence should be addressed. E-mail: [email protected]

Received 25 July 2011; Revised 15 October 2011; Accepted 25 October 2011

Abstract

Like all organisms, plants require energy for growth. They achieve this by absorbing light and fixing it into a usable,

chemical form via photosynthesis. The resulting carbohydrate (sugar) energy is then utilized as substrates for

growth, or stored as reserves. It is therefore not surprising that modulation of carbohydrate metabolism can have

profound effects on plant growth, particularly cell division and expansion. However, recent studies on mutants such

as stimpy or ramosa3 have also suggested that sugars can act as signalling molecules that control distinct aspects

of plant development. This review will focus on these more specific roles of sugars in development, and will

concentrate on two major areas: (i) cross-talk between sugar and hormonal signalling; and (ii) potential directdevelopmental effects of sugars. In the latter, developmental mutant phenotypes that are modulated by sugars as

well as a putative role for trehalose-6-phosphate in inflorescence development are discussed. Because plant growth

and development are plastic, and are greatly affected by environmental and nutritional conditions, the distinction

between purely metabolic and specific developmental effects is somewhat blurred, but the focus will be on clear

examples where sugar-related processes or molecules have been linked to known developmental mechanisms.

Key words: Meristem, plant development, ramosa3, stimpy; sugars, trehalose.

Introduction: translating nutrient status intoplant growth and development

Carbohydrates, or sugars, are essential to the fundamental

processes required for plant growth. Therefore, carbohydrate

production, metabolism, and use must be carefully coordi-

nated with photosynthate availability, environmental cues,

and timing of key developmental programmes. Sugars in

general can act as signalling molecules and/or as global

regulators of gene expression, for example acting like

hormones and translating nutrient status to regulation of

growth and the floral transition (Koch, 1996, 2004; Wobus

and Weber, 1999b; Smeekens, 2000; Ohto et al., 2001;

Rolland et al., 2002, 2006; Price et al., 2004; Smeekens et al.,

2010). Therefore, sugar-responsive gene regulation reflects

carbohydrate abundance or depletion (Koch et al., 1996;

Rolland et al., 2002; Koch, 2004). The translation of nutrient

status to transcriptional regulation allows the plant to

modulate growth, both at the whole plant level and locally,

in tissue- or cell-specific patterns, potentially to coordinate

developmental programmes with available carbohydrate. In

response to sugar depletion, genes involved in photosynthe-

sis, carbohydrate remobilization and export, and nitrogen

(N) metabolism tend to be up-regulated. Alternatively, sugar

abundance induces typical sink organ activities such as

carbohydrate import, utilization, and storage, and starch

and anthocyanin biosynthesis. Comprehensive reviews on

sugar sensing and signalling, carbohydrate allocation, and

growth are available and should be referred to for additionalinformation (Koch et al., 1996; Smeekens, 2000; Rolland

et al., 2002, 2006; Koch, 2004; Ainsworth and Bush, 2011).

Specific growth and metabolic responses tend to be acti-

vated and/or modulated based on the nature of the sugar

signal. For example, sucrose, the primary transport sugar in

plants, can be sensed as a signal directly (Chiou and Bush,

1998) or, alternatively, a signal can arise via its hexose

cleavage products, glucose (glc) or UDP-glc and fructose(Rolland et al., 2002; Price et al., 2004; Li et al., 2011).

A number of genes involved in sugar sensing and signalling

have been identified in mutant screens for altered responses

to exogenous sugars during seed germination and early

seedling growth in Arabidopsis (reviewed in Smeekens, 2000;

The Author [2011]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.For Permissions, please e-mail: [email protected]

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Rolland et al., 2002, 2006; Gibson, 2005). For example, glucose

insensitive (gin) mutants fail to undergo growth arrest in the

presence of inhibitory levels of glc, exhibiting normal

hypocotyl elongation, cotyledon greening, and expansion.

Independent screens for other sugar response phenotypes

revealed that certain sucrose uncoupled (sun), sugar insensitive

(sis), and/or impaired sucrose induction (isi) mutations were

allelic to gin loci, suggesting that these genes may function atthe interface of different sugar signalling pathways (Zhou

et al., 1998; Smeekens, 2000; Rolland et al., 2002; Gibson,

2005). It should be noted, however, that results from such

screens could potentially be secondary responses to hexose

products generated from sucrose-mediated induction of

sucrose-cleaving enzymes such as extracellular invertases.

Additionally, the disaccharide trehalose, and its metabolic

intermediate, trehalose-6-phosphate (T6P), are implicated inthe regulation of specific growth responses (Eastmond and

Graham, 2003; Paul, 2008; Smeekens et al., 2010), and are

discussed in relation to putative roles in development later in

this review.

It is obvious that, in general, metabolism should be

tightly coupled to regulatory mechanisms that control

growth and development, but few examples exist of how

this might occur. Sugar signals can reportedly be generatedeither by carbohydrate concentration and relative ratios to

other metabolites, such as C:N (Coruzzi and Bush, 2001;

Palenchar et al., 2004), or by flux through sugar-specific

sensors and/or transporters (Lalonde et al., 1999, 2004;

Williams et al., 2000; Vaughn et al., 2002; Buttner, 2010).

One possible regulatory mechanism that has come to light

recently is that metabolic enzymes can also function as

active members of transcriptional regulatory complexes.The best example in plants involves hexokinase (HXK),

which, aside from catalysing glc phosphorylation in the first

committed step of glycolysis, also acts as a hexose sensor to

transduce signals based on sugar availability (Jang et al.,

1997; Xiao et al., 2000; Harrington and Bush, 2003; Moore

et al., 2003). Interestingly, hxk1 mutants lacking catalytic

activity are still active in some glc responses (Harrington and

Bush, 2003; Moore et al., 2003), and recently it was found thatsome of the cellular pool of HXK1 protein is present in the

nucleus, where it associates with putative transcriptional

complexes (Cho et al., 2006). Several other examples of

metabolic enzymes, moonlighting as transcriptional regula-

tors, including Arg5,6, which function in yeast arginine

biosynthesis, galactokinase, and glyceraldehyde-3-phosphate

dehydrogenase, have been described in other organisms

(Zenke et al., 1996; Zheng et al., 2003; Hall et al., 2004),indicating that HXK1 is not an isolated example. This

remarkable cross-functionalization presumably enables cross-

talk between metabolic pathways or sensors, and gene

regulation. An additional sensing mechanism that has been

reported involves cell surface receptors of extracellular sugar

signals, such as RGS1, a negative regulator of G-protein

signalling (Chen et al., 2003; Chen and Jones, 2004).

In general, hexoses tend to have greater signallingpotential in promoting organ growth and cell proliferation,

while sucrose is typically associated with differentiation and

maturation (Borisjuk et al., 2002; Koch, 2004). Relative

ratios of hexoses to sucrose are perceived and maintained

by sucrose metabolic enzymes, isoforms of which can act in

a spatiotemporal manner to coordinate and fine-tune

growth during key phases of development (Xu et al., 1996;

Koch, 2004). Sugar metabolic enzymes and transporters can

thus function in establishing sugar gradients within tissues

(Weschke et al., 2000, 2003). Previous work in developinglegume embryos showed that differential glc concentrations

along a spatial gradient correlated with increased mitotic

activity (Borisjuk et al., 1998, 2003), suggesting a link

between hexoses and the cell cycle. Consistent with this,

sugars have been shown to control cell division through

modulation of cyclinD (CycD) gene expression (Riou-

Khamlichi et al., 1999, 2000; Gaudin et al., 2000).

While availability of carbohydrate substrates required fororgan growth naturally has an impact on plant development,

sugars can also cross-talk with known phytohormone signal-

ling networks to modulate critical growth processes such as

embryo establishment, seed germination, and seedling and

tuber growth (Gazzarrini and McCourt, 2001; Rolland et al.,

2002, 2006; Leon and Sheen, 2003; Gibson, 2004, 2005).

There is also increasing evidence that sugars can regulate

specific developmental programmes and transitions via genesthat control meristem maintenance and identity (Wu et al.,

2005; Satoh-Nagasawa et al., 2006). Meristems are pluripo-

tent stem cell populations, which can either divide indefinitely

or respond to positional cues that direct the developmental

fate of new plant organs. Because of a strong carbohydrate

requirement in dividing and differentiating cells, it makes

sense that meristem maintenance, identity, and organogen-

esis should be carefully coordinated with nutrient status(Francis and Halford, 2006). Indeed, Pien et al. (2001)

observed spatiotemporal expression of carbohydrate meta-

bolic genes in the tomato shoot apical meristem (SAM) and

developing leaf primordia. In Arabidopsis, misexpression of

a specific extracellular invertase, which cleaves sucrose into

glc and fructose, in the SAM caused changes in flowering

time and inflorescence architecture (Heyer et al., 2004). In

addition, sucrose can rescue flowering time mutant pheno-types, through control of meristem identity genes, such as

LEAFY (Ohto et al., 2001). Recent work has also shown

that exogenous sucrose can compensate for regulators of

meristem maintenance in the shoot (Wu et al., 2005) (see

later discussion) and root (Wahl et al., 2010).

Potential roles of sugars in regulating specific develop-

mental programmes are highlighted in this review. Since

hormonal cues are imperative in maintaining meristemintegrity and establishing developmental fate, known exam-

ples of cross-talk between sugar and hormone signalling

pathways in modulating plant growth are also discussed. In

addition, how sugarhormone connections might regulate

certain developmental processes is considered. Additional

important examples of sugar signalling factors that have

been suggested to control plant growth, such as the TOR

kinase, SNF1-related kinase, and C/S1 bZip factors, havebeen discussed in a recent review (Smeekens et al., 2010),

and will not be discussed here.

2 of 11 | Eveland and Jackson

Cross-talk between sugar and hormonesignalling

Sugar-based signalling pathways cross-talk with various

hormones to modulate critical aspects of plant growth. In

general, plants defective in abscisic acid (ABA) and/or

ethylene perception and signalling tend to display altered

sugar response phenotypes. Therefore, comparable mutantscreens and subsequent genetic and functional analyses have

revealed extensive overlap between sugar, ABA, and ethylene

signals in controlling processes such as seed germination and

seedling growth, as reviewed in Gazzarrini and McCourt

(2001), Gibson (2004, 2005), Leon and Sheen (2003), and

Rolland et al. (2002, 2006). However, additional connections

between sugars and other plant hormones, such as auxin,

have emerged, and some evidence suggests potential sugarhormone regulation of specific developmental processes.

Here, findings that have established mechanisms of sugar,

ABA, and ethylene cross-talk during plant growth are

highlighted, and an emerging role for sugarauxin interac-

tions in growth and development is also discussed.

Sugar, ABA, and ethylene signalling networks convergeto control plant growth

Initial evidence for sugar and ABA cross-talk came from

observations that a number of mutants identified in sugar

response screens were also defective in ABA metabolism or

response. For example, certain ABA biosynthesis (aba) andABA-insensitive (abi) mutants are insensitive to high glc

(Arenas-Huertero et al., 2000; Brocard et al., 2002; Leon

and Sheen, 2003; Dekkers et al., 2008). Extensive cross-talk

between sugar and ABA signalling pathways has therefore

been described for various aspects of plant growth and

metabolism (Gazzarrini and McCourt, 2001; Finkelstein

and Gibson, 2002; Gibson, 2004, 2005). Sugars and ABA

tend to act synergistically during embryo growth, intransitioning from a phase of rapid cell division to cell

enlargement and accumulation of storage reserves (Wobus

and Weber, 1999a, b; Finkelstein and Gibson, 2002). For

example, ABA enhances sucrose induction of starch bio-

synthetic genes (Rook et al., 2001). Alternatively, ABA and

glc act antagonistically during seed germination and early

seedling growth, where exogenous glc enables wild-type

Arabidopsis seeds to germinate on otherwise inhibitoryABA concentrations (Leon and Sheen, 2003).

A direct link between sugar signalling and hormone

biosynthesis was revealed by characterization of ABA bio-

synthetic genes, ABA1ABA3, which were also independently

isolated as gin mutants (Arenas-Huertero et al., 2000; Laby

et al., 2000; Rook et al., 2001). Exogenous glc can increase

both expression of these ABA synthesis genes and, conse-

quently, endogenous ABA levels (Cheng et al., 2002). A keylink between sugars and ABA perception is exemplified by

ABI4, which encodes an AP2 domain transcription factor

and is required for normal sugar response during germina-

tion and seedling growth (Arenas-Huertero et al., 2000;

Huijser et al., 2000; Laby et al., 2000; Rook et al., 2001). In

maize seeds, ABI4 is regulated by sugar in the developing

embryo, and binds regulatory elements for both ABA and

sugar (Niu et al., 2002). Interestingly, not all ABI genes are

responsive to sugars, suggesting multiple ABA signalling

pathways at work (Laby et al., 2000; Dekkers et al., 2008).

Genome-wide analysis tools are currently being used to

resolve additional players in the sugarABA signalling

network(s) (Li et al., 2006). For example, recent workidentified a splicing factor, SR45, as a negative regulator of

sugar signalling during early seedling growth. SR45 is

involved in the repression of glc-induced ABA accumulation,

and down-regulation of genes for ABA biosynthesis and

signalling (Carvalho et al., 2010).

Ethylene sensing and signalling pathways are also tightly

interconnected with those for sugar and ABA (Gazzarrini

and McCourt, 2001; Leon and Sheen, 2003). Mutants inethylene perception, ethylene receptor 1 (etr1) and ethylene

insensitive 2 and 3 (ein2 and ein3), are glc hypersensitive,

while constitutive triple response 1 (ctr1), a negative regulator

of ethylene signalling, is glc insensitive (Zhou et al., 1998;

Gibson et al., 2001; Yanagisawa et al., 2003). While basic

models have been suggested for regulatory mechanisms

among these pathways, hormone signals may differentially

affect gene expression depending on sugar concentration,localization, or the nature of the sugar signal. Glc and

ethylene signalling pathways tend to act antagonistically,

partially through repression of ABA biosynthetic genes. For

example, ABA levels are enhanced in the ein2 mutant, and

wild-type seedlings treated with the ethylene precursor

1-aminocyclopropane-1-carboxylic acid (ACC) phenocopy

gin mutants (Ghassemian et al., 2000). Interestingly, ethylene

also appears to play a role in root meristem maintenance(Ortega-Martinez et al., 2007), via a mechanism that

possibly involves auxin. Evidence for the latter includes

attenuation of ethylene effects in roots of certain auxin

mutants (Ortega-Martinez et al., 2007), and ethylene-

induced expression of auxin biosynthetic genes in the root

meristem (Stepanova et al., 2008). Whether sugar signals

contribute to ethylene- and auxin-based regulation in root

meristem maintenance remains to be determined; however,additional evidence relates sugar and auxin signals to root

development, and is discussed below.

Emerging roles for sugarauxin cross-talk during plantgrowth and development

Auxin is an important plant hormone that can act as a general

regulator of growth and is also implicated in pattern

formation, lateral organ development, and cell expansion

(reviewed by Hamant et al., 2010; Kieffer et al., 2010).

Directional transport and local accumulation of auxin in

spatiotemporal gradients regulate these developmental pro-

cesses. Auxin biosynthesis and response pathways are alsointerconnected with those of other hormones, such as ethylene,

brassinosteroids, and cytokinins (Kieffer et al., 2010). Evi-

dence linking sugar and auxin signals is also emerging in

various aspects of plant growth and development. Initial work

on hxk/gin2 in Arabidopsis showed that the mutants displayed

Sugars, signalling, and plant development | 3 of 11

resistance to exogenous auxin, and that auxin-resistant

mutants were insensitive to high glc (Moore et al., 2003). In

addition, hxk-based signalling positively and negatively inter-

acts with auxin and cytokinin, respectively (Moore et al., 2003;

Rolland et al., 2006). More recently, a novel allele of hookless1

(hls1) was shown to be resistant to both sugar and auxin

responses, suggesting it may partially function in negative

effects of auxin on sugar-responsive gene expression (Ohtoet al., 2006). In developing maize kernels, an auxin bio-

synthetic gene, ZmYUCCA, was recently reported to be

modulated by sugar, representing a link between sugar status

and auxin signals (LeClere et al., 2010). An interesting

connection between polar auxin transport and sucrose metab-

olism was also described during the maize stem gravitropism

response. Here, auxin redistribution was necessary for grav-

istimulated sucrose hydrolysis in generating an asymmetrichexose gradient, which caused differential cell elongation in

cells of the internodal pulvinus (Long et al., 2002).

A genome-wide expression profiling study by Mishra

et al. (2009) showed substantial overlap of glc and auxin

response pathways controlling root growth and develop-

ment in Arabidopsis seedlings. Here, 62% of genes affected

by auxin were regulated by glc, and in many instances glc

and auxin acted either antagonistically or synergistically toregulate transcription. While increasing concentrations of

glc induced genes for auxin biosynthesis and transport, they

had differential effects on individual auxin receptors (Mis-

hra et al., 2009). Interestingly, a number of auxin-regulated

genes that did not respond to glc alone were modulated by

glc in the presence of auxin. Notably, these included AUX/

IAA and Lateral Organ Boundary (LOB) domain gene

family members. In addition, exogenous glc significantlyaccentuated defects in lateral root induction, root hair

elongation, and gravitropism in auxin sensing and signalling

mutants, suggesting that glc may affect root architecture

through auxin-based signal transduction (Mishra et al.,

2009). Another study in Arabidopsis roots showed that

expression of a WUSCHEL (WUS)-related homeobox gene,

WOX5, which maintains localized auxin maxima in the root

apical meristem, is induced by auxin and turanose, a non-metabolizable sucrose analogue (Gonzali et al., 2005).

Specific developmental pathways involvingsugars

In this section the focus is on examples where sugars have

been linked to specific developmental processes or path-

ways. How sugars may play a regulatory role in maintain-

ing meristem function, via action of key developmentalgenes, and emerging views on how trehalose-based signal-

ling may be involved in plant development, are discussed.

Shoot meristem maintenance and sugars: stimpy

stimpy (stip) is a mutant in WOX9, a homeobox gene related

to WUS, a gene expressed in the organizing centre of the

SAM and required for maintenance of shoot stem cells. stip

mutants mostly arrest soon after germination (Fig. 1A), and

also have SAM defects, possibly as a result of defective WUS

expression. This effect appears to be more general than the

role of WUS in stem cell/organizing centre specification, and

it is thought that STIP functions by maintaining cell division

in root as well as shoot development. Remarkably, stip

mutants can be rescued by addition of sucrose, and the

mutants, once rescued, can undergo normal growth anddevelopment. Sucrose thus can compensate for loss of a gene

that is typically required for normal meristem development

(Fig. 1). While the exact reason for sucrose rescue is not

clear, one possibility is that it acts by promoting cell division

through up-regulation of CycD expression (Riou-Khamlichi

et al., 2000). This could reflect a cross-talk with cytokinin

signalling, which also induces CycD expression (Riou-

Khamlichi et al., 1999). Additional insight into the role ofcytokinins comes from the observation that they are required

for activation of stip expression, linking cytokinin signalling

to meristem establishment through the action of stip (Skylar

et al., 2010). Recently, characterization of the plant-specific

FANTASTIC FOUR (FAF) genes, which encode proteins of

unknown function, uncovered a putative role for FAF2 and

FAF4 in controlling shoot meristem size and maintenance of

meristem function, working through WUS (Wahl et al.,2010). In contrast to STIP, the overexpression of FAF2 or

FAF4 arrests shoot and root growth shortly after germina-

tion, and root growth arrest can also be rescued by addition

of exogenous sucrose. Although further work is needed to

understand the connection between these genes, it was

proposed that STIP and FAF genes might play antagonistic

roles in translating sugar signals to meristem maintenance

(Wahl et al., 2010).

Trehalose signalling and development: RAMOSA3 andmeristem determinacy

Trehalose is a disaccharide that is present in all kingdoms,

and functions in microbes and invertebrates in carbohydratestorage, transport, signalling, and stress protection (Elbein,

1974; Crowe et al., 1992; Strom and Kaasen, 1993; Paiva and

Panek, 1996). At one time, it was thought that the occurrence

of trehalose in plants was limited to specialized, desiccation-

tolerant species (Muller et al., 1995). However, genome

Fig. 1. Sugars rescue stimpy (stip) mutants. stip mutants of

Arabidopsis are embryo/early seedling lethal when grown in plates

without an exogenous carbon source (A). However, they recover

when grown on plates with added sucrose (B). Reproduced from

Current Biology, 15, Wu X, Dabi T, Weigel D. Requirement of

homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth

and maintenance. 436440. Copyright 2005 with Permission of

Elsevier.


sequences revealed trehalose biosynthetic genes in all plants

(Leyman et al., 2001; Muller et al., 2001; Vogel et al., 2001).

In most plants, however, trehalose is present at low

micromolar concentrations, suggesting a regulatory rather

than a metabolic role (Paul et al., 2008).

The biosynthesis of trehalose in plants occurs in two steps

(Goddijn and van Dun, 1999; Paul et al., 2008). First, the

intermediate, trehalose-6-phosphate (T6P), is formed fromUDP-glc and glc-6-phosphate by trehalose-6-phosphate syn-

thases (TPSs). Next, T6P is converted to trehalose by

trehalose-6-phosphate phosphatases (TPPs) (Cabib and Leloir,

1958) (Fig. 2). In Saccharomyces cerevisiae, and Escherichia

coli, TPS and TPP are single-copy genes (Londesborough and

Vuorio, 1991; Kaasen et al., 1992, 1994; Bell et al., 1998),

whereas plants encode multiple homologues of each (Leyman

et al., 2001; Paul et al., 2008). Functional analysis of the plantTPS genes has concentrated on TPS1. Arabidopsis tps1 loss-

of-function mutants are embryo lethal, and use of misexpres-

sion or weak alleles has shown that TPS1 function is required

throughout the plant life cycle; weak alleles have slow growth

and delayed flowering (Eastmond et al., 2002; van Dijken

et al., 2004; Gomez et al., 2010). tps1 mutants cannot be

rescued by exogenous trehalose, suggesting that the intermedi-

ate T6P is important (Eastmond et al., 2002). In itself, theobservation that tps1 mutants are embryo lethal does not

prove a developmental role for this gene, because many

housekeeping genes encoding basic cellular functions in

plants also have embryo lethal phenotypes (Tzafrir et al.,

2004), and TPS1 appears to encode the only functional TPS

enzyme in Arabidopsis (Vandesteene et al., 2010). Arabidop-

sis also contains 10 TPP genes, with conserved phosphatase

motifs typical of this class of phosphohydrolases (Thaller

et al., 1998). Two of these genes were first isolated by

complementation of yeast tps2 mutants (Vogel et al., 1998),

suggesting they have TPP function. Little other informationis available on the biological roles of the TPP genes,

although two of them might be regulated by the stem cell

regulator WUS in Arabidopsis, pointing to possible de-

velopmental roles (see supplementary data in Leibfried

et al., 2005). Plants also encode some genes that have both

TPS- and TPP-like domains, though they appear to lack

either TPS or TPP enzymatic activity and might rather

function as regulatory or sensor proteins (Lunn, 2007;Ramon et al., 2009). An Arabidopsis mutant in one of

them, AtTPS6, was found to have interesting cell shape

defects, pointing to a possible role for trehalose signalling

in cell fate specification (Chary et al., 2008).

Insights into potential developmental effects of the

trehalose pathway have come from heterologous expression

studies. For example, plants overexpressing microbial

trehalose biosynthetic genes were found to have alteredcarbohydrate metabolism and morphological defects, such

as stunted growth and lanceolate leaves (Romero et al.,

1997; Garg et al., 2002; Schluepmann et al., 2003, 2004).

Fig. 2. The trehalose biosynthetic pathway and mutant phenotypes. (a) Trehalose is produced by two enzymatic reactions, via the

intermediate trehalose-6-phosphate. Compared with wild-type Arabidopsis embryos (b), tps1 mutant embryos are embryo lethal (c)

(EM= embryo; CE= cellular endosperm) (from Eastmond PJ, van Dijken AJ, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JD,

Smeekens SC, Graham IA. 2002. Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for

Arabidopsis embryo maturation. The Plant Journal, with permission of John Wiley and Sons). Wild-type maize ears (d) are unbranched,

whereas ramosa3 mutant ears have abnormal long branches at their base (e, f, branches false coloured in red). The trehalose phosphate

phosphatase, RAMOSA3, is expressed at the base of spikelet pair meristems in developing maize ears [black signal, in situ hybridization

in (g); red signal is in situ hybridization of KNOTTED1, marking the meristem cells (Satoh Nagasawa and Jackson, unpublished)]. (h) A

pathway for maize inflorescence branch determinacy, showing that RA3 and RA2 act in parallel and upstream of RA1 (based on

Vollbrecht et al., 2005; Satoh-Nagasawa et al., 2006).


These phenotypes are thought to result from changes in

carbon allocation between sink and source tissues (Eastmond

and Graham, 2003), and provoked speculation that trehalose

may be involved in sugar signalling (Goddijn and van Dun,

1999; Paul et al., 2008). One possible target of the putative

trehalose signal is ADP-glc pyrophosphorylase, which cata-

lyzes the first committed step in starch biosynthesis (Wingler

et al., 2000; Lunn et al., 2006). Recent evidence points to theintermediate T6P, rather than trehalose itself, as the key

regulatory signal (Schluepmann et al., 2003, 2004; Lunn

et al., 2006; Paul et al., 2008). T6P appears to act as

a regulator of carbon metabolism, and, remarkably, as an

enhancer of photosynthetic capacity (Paul et al., 2001;

Eastmond and Graham, 2003). Paul et al. (2001) reasoned

that T6P could be the signal that allows HXK to perceive

carbon status, as in yeast (Thevelein and Hohmann, 1995);however, T6P is not an inhibitor of Arabidopsis HXKs

(Eastmond et al., 2002). More recent data point to a link

between T6P induction by sucrose and promotion of growth

(Lunn et al., 2006), although T6P is also a potent growth

inhibitor in the absence of exogenous carbon sources

(Schluepmann et al., 2003, 2004). It is becoming clear that

T6P levels provide an important signal that links plant

metabolism with growth and development, though how thisoccurs is not fully understood (Paul et al., 2008). However,

a recent advance identified SnRKs (Snf1-related protein

kinases), which integrate energy signalling and growth in

plants, as possible T6P targets (Baena-Gonzalez et al., 2007).

SnRK1 activity is specifically inhibited by T6P in seedling

extracts, but not in immunopurified extracts, suggesting the

presence of an as yet unidentified intermediary factor (Zhang

et al., 2009). Related SnRKs act as important regulators ofcentral carbon and nitrogen metabolism, and link nutrient

stress to a number of response pathways (Halford and Hey,

2009; Smeekens et al., 2010). In addition, Arabidopsis lines

that overexpress the bZIP11 transcription factor were

identified in an elegant screen to isolate genes that suppress

growth inhibition by trehalose (Delatte et al., 2011). bZIP11,

which itself is both induced by sucrose at the transcriptional

level and repressed by sucrose at the translational level (Maet al., 2011), is therefore another important signalling

component in this network (Delatte et al., 2011). It will thus

be interesting to further establish connections among these

sugar-based signalling modules.

A surprising insight into a potential role for trehalose

signalling in development came from the discovery that the

maize inflorescence developmental gene RAMOSA3 encodes

a functional TPP enzyme (Satoh-Nagasawa et al., 2006).Inflorescence morphology is strongly impacted by axillary

meristem initiation and growth patterns (Prusinkiewicz et al.,

2007; Prenner et al., 2009). In the grasses, inflorescence

development is characterized by the formation of short

branches called spikelets that contain the floral structures,

the florets (Irish, 1998; Bommert et al., 2005; Doust, 2007).

Maize forms two distinct types of inflorescences; the terminal

tassel has long basal branches and develops the male flowers,and the axillary ears, which have a prominent axis lacking

long branches, and develop female flowers. In each structure,

development proceeds by the initiation of spikelet pair

meristems (SPMs) on the flanks of the inflorescence meristem

(IM); seen in scanning electron micrographs (Fig. 2f). Each

SPM develops into a short axillary branch, bearing two

spikelet meristems, which in turn initiate two floral meris-

tems. In the tassel, the IM also initiates several branch

meristems, which are indeterminate, and grow out to make

the long branches at the base of the tassel (Cheng et al., 1983;Bommert et al., 2005; Doust, 2007).

Inflorescence morphology in the grasses is highly variable

(Bommert et al., 2005; Doust, 2007), and a large factor

controlling this variability is the developmental control of

axillary meristem determinacy. In maize, this determinacy

decision is controlled by the RAMOSA genes, RA1, 2, and

3. RAMOSA (RA) genes (from the Latin ramus, meaning

branch) control axillary meristem growth by imposingdeterminacy, and consequently ra loss-of-function mutants

have more indeterminate, highly branched inflorescences

(McSteen, 2006; Vollbrecht and Schmidt, 2008). RA1

encodes a putative C2H2 zinc finger transcription factor

that appears to have played a key role in maize domestica-

tion and grass evolution (Vollbrecht et al., 2005). RA2 also

encodes a putative transcription factor, a LOB domain

protein (Bortiri et al., 2006), whereas RA3 encodes a func-tional TPP enzyme (Satoh-Nagasawa et al., 2006). Interest-

ingly, genetic and molecular studies suggest that both RA2

and RA3 are required for proper RA1 expression (Voll-

brecht et al., 2005; Bortiri et al., 2006; Satoh-Nagasawa

et al., 2006) (Fig. 2h). All three genes are expressed in

overlapping domains: RA2 is expressed in the axillary

meristems themselves (Bortiri et al., 2006), whereas RA1

and RA3 expression is only at the base of these meristems,suggesting that they may control a mobile signal that

regulates meristem determinacy (Vollbrecht et al., 2005;

Satoh-Nagasawa et al., 2006).

RA3 is a functional TPP enzyme, since the bacterial-

expressed protein has specific activity for T6P, and the

protein can complement a yeast TPP mutant, suggesting

a role for trehalose signalling in meristem determinacy

(Satoh-Nagasawa et al., 2006). However, the fact that RA3controls levels of RA1 expression in the genetically defined

RAMOSA mutant pathway suggests that RA3 might have

an alternative regulatory function. One hypothesis is that

RA3, like some metabolic enzymes in yeast (Zenke et al.,

1996; Zheng et al., 2003; Hall et al., 2004), and HXK in

Arabidopsis (Cho et al., 2006), might play a moonlighting

role in transcriptional regulation, as discussed earlier.

Whatever the mechanism of RA3 action is, it is clear thatthis pathway is not specific to maize. A rice homologue of

RA3 (Os SRA) has a similar, highly localized expression at the

base of inflorescence branches (Satoh-Nagasawa et al., 2006).

Some Arabidopsis TPP family members also have restricted

expression patterns during inflorescence development, similar

to RA3, suggesting that a similar pathway might control

Arabidopsis inflorescence architecture (S. Goldshmidt and DJ,

unpublished).Insights into potential regulatory mechanisms of RA3 were

gained through genome-wide transcript profiles, comparing


wild-type developing ear primorida with those from loss-of-

function ra3 mutants (Eveland et al., 2010). Here, a number of

genes that showed differential expression in the ra3 back-

ground were associated with metabolic pathways for primary

carbohydrate biosynthesis and degradation, energy produc-

tion, and trehalose metabolism, suggesting global effects of

sugar status associated with altered TPP activity. In addition,

consistent with a putative role for RA3 in transcriptionalregulation, developmentally regulated transcription factors

were also misexpressed in the ra3 mutants. Among these were

genes related to various hormone sensing and signalling

pathways, such as auxin and ethylene, including nine ethyl-

ene-response factor (ERF) family members, as well as genes

involved in brassinosteroid signal transduction (Eveland et al.,

2010). Testable hypotheses that emerge from genome-wide

studies such as this will enable further resolution of functionalroles for RA3, including potential connections to sugar signals

and/or overlaps with hormone-sensing pathways, and how

sugarhormone cross-talk may contribute to the genetic

control of plant development.

Summary

Sugars are essential, and so genetic approaches to un-

derstanding their roles in plant development are compli-cated. Sugar-related mutants might be embryo lethal, but

this could indicate either a developmental defect or simply

a critical metabolic or housekeeping function. Mutants are

also likely to be pleiotropic, because they could induce

general growth defects. New insights will come from

identifying mutants, such as stip or ra3, that have specific

developmental functions, and assembling these mutants into

known developmental pathways, using classical geneticsand/or genomics approaches, and also from integrating

genomic data from sugar signalling and developmental

mutants.

Acknowledgements

Research on this topic is supported by grants from the

National Science Foundation (DBI-06049123 and MCB-

1027445). Thanks to Morgan Xianfeng Xu and Stacy

DeBlasio for critical reading of the manuscript.

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Sugars, Signalling, And Plant Development