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Sugar and hormone connections

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Sugar and hormone connectionsSugar-signalling mutants reveal the hormone connectionsGlucose controls ABA biosynthesis genesGlucose controls ABA signalling genesDistinct glucose and osmotic-stress signallingGlucose and ABA in growth promotion and inhibitionGlucose and ethylene connectionsConclusions and perspectivesAcknowledgementsReferencesSugar and hormone connectionsPatricia Leo´n1and Jen Sheen21Departamento de Biologı´a Molecular de Plantas, Instituto de Biotecnologı´a, Universidad Nacional Autonoma de Me´ xico,Cuernavaca, Morelos 62271, Mexico2Department of Genetics, Harvard Medical School, and Department of Molecular Biology, Massachusetts General Hospital, Boston,MA 02114, USASugars modulate many vital processes that are alsocontrolled by hormones during plant growth and devel-opment. Characterization of sugar-signalling mutantsin Arabidopsis has unravelled a complex signalling net-work that links sugar responses to two plant stresshormones – abscisic acid and ethylene – in oppositeways. Recent molecular analyses have revealed direct,extensive glucose control of abscisic acid biosynthesisand signalling genes that partially antagonizes ethylenesignalling during seedling development under light.Glucose and abscisic acid promote growth at low con-centrations but act synergistically to inhibit growth athigh concentrations. The effects of sugar and osmoticstress on morphogenesis and gene expression are dis-tinct. The plasticity of plant growth and developmentare exemplified by the complex interplay of sugar andhormone signalling.The role of sugars as signalling molecules has been widelyrecognized in microorganisms and has recently emerged inanimals and plants [1]. During plant growth and devel-opment, sugars modulate a range of vital processes such asseed germination, seedling development, root and leafdifferentiation, floral transition, fruit ripening, embryo-genesis, and senescence, as well as responses to light,stress and pathogens [2–9]. Based on the differentresponses that diverse genes exhibit to particular sugarsor sugar-phosphorylation activities, the existence ofmultiple signal-transduction pathways has been proposed[6,7]. Currently, it is unclear whether these signallingpathways interconnect or whether they function in specificcell types or at specific developmental stages. To addressthese types of questions, it is necessary to understand intemporal and spatial detail the mechanisms by whichsugar signals are transduced in each pathway and thenature of the molecules that participate in these processes.In an effort to understand the molecular mechan-isms involved in the sugar perception and signallingnetwork, genetic strategies have been designed inde-pendently to select either sugar-insensitive or sugar-oversensitive mutants, mainly in Arabidopsis. The geneticscreens are reminiscent of those devised for the isolation ofplant hormone mutants. By using easily detectablephenotypes such as the sugar inhibition of germinationor postgermination development in seedlings, mutantswith altered sugar responses have been isolated andcharacterized [10–15]. Sugar-response mutants have alsobeen isolated by screening transgenic seedlings carryingreporter and selection genes under the control of sugar-regulated promoters [16,17]. These distinct screeningstrategies yielded overlapping mutants. Surprisingly,characterization of these mutants has led to the identifi-cation of mutants and genes previously implicated inplant-hormone biosynthesis or signalling, and revealedextensive connections between the sugar and plant-hormone pathways [18]. The aim of this article is tohighlight the latest findings that might provide somemolecular insights into the intricate network of plantsugar signalling and its direct, extensive relationship toabscisic acid (ABA) and ethylene hormonal pathways.Sugar-signalling mutants reveal the hormoneconnectionsRecent genetic and molecular studies of sugar-signallingmutants in Arabidopsis have uncovered many unexpectedlinks between sugar and plant-hormone signalling (Table 1).In addition to the altered sugar responses (Fig. 1), thesemutants display phenotypes found in ABA or ethylenebiosynthesis mutants and in ABA or ethylene signallingmutants (Fig. 2). For example, the small, dark-green leavesof the gin1 mutant, resembling the constitutively activeethylene mutant ctr1 (Fig. 2), prompted the application ofan ethylene precursor 1-aminocyclopropane-1-carboxylateFig. 1. Arabidopsis glucose-insensitive (gin) mutants. Seedlings were grown on6% glucose– Murashige and Skoog (MS) medium for 4–5 days under constantlight. (a) Wild type (WT). (b) The glucose-insensitive phenotype can be mimickedby treatment with the ethylene precursor 1-aminocyclopropane-1-carboxylate(ACC). (c) Abscisic acid-deficient gin1 (aba2) and (d) constitutive ethylene-signal-ling gin4(ctr1) mutants display a similar glucose-insensitive phenotype except forroot elongation. (e) Endogenous abscisic acid is required for the glucose-oversen-sitive phenotype of the ethylene-insensitive mutant ein2 because (f) the gin1 ein2double mutant exhibits the glucose-insensitive phenotype.(a) (b) (c) (d) (e) (f)WT WT + ACCgin1(aba2)gin4(ctr1)ein2 gin1 ein2doublemutantCorresponding author: Jen Sheen ([email protected]).Opinion TRENDS in Plant Science Vol.8 No.3 March 2003110http://plants.trends.com 1360-1385/03/$ - see front matter q 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S1360-1385(03)00011-6(ACC) to wild-type plants in the presence of excessexogenous glucose. This experiment demonstrated thatthe glucose-dependent developmental arrest could beovercome by ethylene (Fig. 1) [12]. Although ethylene isgenerally known as a stress hormone that inhibits growth,this study reveals a growth-promoting role of ethylene inArabidopsis. Interestingly, the ctr1 mutant produces manymore leaves than wild-type plants even in the absence ofexogenous glucose (Fig. 2). It was also found that thesugar-insensitive gin1 and gin5 mutants had reduced-seed-dormancy and wilty phenotypes that are character-istics of ABA-deficient (aba) mutants [13,19]. Thesefindings led to an awareness of the important geneticinteractions between the sugar and ABA, and between thesugar and ethylene signalling pathways [12–14,16,17,19].The molecular cloning of GIN6/SUN6 as ABI4 andGIN1/ISI4 as ABA2 strengthened the molecular connec-tions between sugar and ABA [13,16,17,19]. Geneticanalyses also confirmed that


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