Sugar hormonal and environmental signalling crosstalk

Sugar signalling often inter-connects with hormone-induced pathways to modulate gene expression and physiological processes along plant life. In Arabidopsis, interactions between sugar and ABA signalling have been mostly studied during early seedling development through the characterization of mutants. Many of these mutations affecting sugar signalling are allelic with components of ABA synthesis or ABA transduction pathway (Leon and Sheen 2003, Rook and Bevan 2003, Gibson 2004). Glucose induces a specific accumulation of ABA during this stage of plant life, an essential increase for the plant to potentiate the efficiency of sugar signals (Rolland et al. 2006). In grape, ABA and sugars, both accumulating during berry ripening, affect important physiological processes in a coordinated manner, such as anthocyanin production and hexose transport. Indeed, in spite of some contradictory reports, it appears that sucrose and ABA act positively on polyphenols and anthocyanins accumulation (Pirie and Mullins 1976, Larronde et al. 1998, Vitrac et al. 2000, Hiratsuka et al. 2001).

A cross-talk between ABA and glucose metabolism is also suggested to enhance phenolics production (Weiss 2000). Furthermore, ABA induces the expression of VvHT1 (Atanassova et al. 2003) and acts synergistically with sugars (sucrose and glucose at physiological concentrations) to transiently induce VvHT1 transcription. In fact, VvHT1 response to both signals involves the presence in its promoter of the cis-element S3S1, a specific overlapping configuration of the two sugar response cis-elements Sucrose box 3 and SURE1. S3S1 constitutes a target for the fixation and the action of the VvMSA (V. vinifera

Maturation, Stress Abscisic acid-induced, also known as VvASR, Vitis vinifera Abscisic acid, Stress, Ripening-induced, AF281656) protein. VvMSA gene expression is strongly upregulated by the combined effect of sugars and ABA and VvMSA enhances VvHTl promoter activity (£akir et al. 2003).

ASRs are globular and highly hydrophilic proteins identified in many plant species but absent from A. thaliana and some other members of the Brassicaceae family (Carrari et al. 2004, Shkolnik and Bar-Zvi 2008). They are involved in abiotic stress (water deficit, salt stress) responses, senescence, pollen maturation and fruit ripening and they respond to ABA, a phytohormone involved in water deficit stresses (Iusem et al. 1993, Kalifa et al. 2004b, Yang et al. 2005), but the different homologues so far identified have different expression patterns, which are organ-specific (Maskin et al. 2001, Frankel et al. 2006). They are small enough to enter the nuclear pore and some, but not all so far identified ASRs, possess a C-terminal nuclear localization signal sequence. However, this signal is neither a sufficient nor exclusive condition for the targeting of the protein to the nucleus. Indeed, regardless the presence of a nuclear targeting signal, most ASR proteins are localized in the cytosol and the nucleus, and some are able to bind to DNA (Carrari et al 2004). Their role as transcription regulators was first evidenced in grape (£akir et al. 2003) and confirmed in tomato (Kalifa et al. 2004a, Rom et al. 2006).

Indeed, the tomato ASR1 (SIASR1) is a DNA binding zinc-dependent protein that preferentially binds to the C2-3(C/G)A sequence (Kalifa et al. 2004a). The potato ci21A/Asr1 plays also a role in the control of hexose transport in heterotrophic organs, since when overexpressed, the tubers display reduced levels of plasma membrane HT mRNAs and consequently lower glucose uptake rates (Schneider et al. 1997, Frankel et al. 2007).

Recent data indicate that SIASR1 competes with ABI4 transcription factor for binding the promoter CE1 cis-acting element, and that the overexpression of SIASR1 in Arabidopsis results in an abi4 phenotype (Shkolnik and Bar-Zvi 2008). ABI4 transcription factors are involved in ABA sensitivity in Arabidopsis seedlings and many abi4 allelic mutations were discovered while screening for mutants impaired in sugar and salt signalling, suggesting that the ABI4 protein is a cross-road between these pathways (Finkelstein et al. 1998, Quesada et al. 2000, Niu et al. 2002, Barrero et al. 2006). Indeed, a common feature for all ASR proteins is their response to ABA.

In grape suspension cultured cells, VvASR expression is strongly enhanced by the addition of ABA. In ripening berries, ABA and sugars accumulate simultaneously after veraison and it is tempting to associate the high expression of VvASR at this time with the presence of both compounds. One should keep in mind however, that the expression patterns displayed by VvASR and VvHT1 in grape berry along ripening are strictly opposite to each other, which, together with the role of VvASR on VvHTVs transcription, can consti tute a brain-teasing problem. Interestingly, the potato ASR ci21A/Asr1 (orthologue of tomato Asr1) expression is also negatively correlated with HT mRNAs accumulated along fruit maturation (Frankel et al. 2007).

However, it is important to recall that positive effect of VvASR on VvHT1 transcription was demonstrated in tobacco, a heterologous system where the protein may not have been in contact with its natural partners. Furthermore, in the light of recent results (Shkolnik and Bar-Zvi 2008), it is possible that VvASR, as SIASR1, is able to compete with other transcription factors for preferred promoter binding sites. Eventually, additional roles, such as a modulation of DNA topology at the image of non-histone chromosomal proteins in response to water and salt stresses, as well as a protective role against water loss cannot be ruled out. ASRs are members of hydrophilins proteins, and enhance water retention once over-expressed, due to their highly hydrophilic nature (Gilad et al. 1997, Koag et al. 2003, Carrari et al. 2004, Kalifa et al. 2004b, Yang et al. 2005, Frankel et al. 2007, Maskin et al. 2007).

Additional connections with the sugar signalling pathways are demonstrated mostly in Arabidopsis with hormones, such as auxins and gibberellins (GAs), cytokinins, ethylene and brassinosteroids. The connection occurs either through the allelic mutation of a gene or the involvement of common cis-acting elements: the AMYBOX2 (TATCCA) sequence is also involved in GAs sensitivity of the a-Amy3 gene encoding for an amylase in rice (Gubler and Jacobsen 1992). The DRE-related element (Drought Response Element) conferred glucose-, ABA- and water stress response (Seki et al. 2007). Recent data reported by Li and co-workers (2006) propose a detailed study of cis-acting elements that confer gene response to glucose and ABA or light signalling as well as transcription factors involved in A. thaliana. Indeed, their microarray studies demonstrate the close connection between these pathways at the levels of promoter, trans-acting elements and gene expression patterns.

In A. thaliana, the hlsl mutant is affected in both sugar and auxin signalling (Ohto et al. 2006). In grape berry and tomato fruit, an early treatment with auxin delays the accumulation of both sugars and secondary metabolites (Cohen 1996, Davies et al. 1997). Besides its positive effect on anthocyanin production, ethylene induces the expression of the sucrose transporters VvSUCll and VvSUC12 and sugar accumulation in grape (Chervin et al. 2006). Furthermore, this climacteric-associated hormone upregulates the alcohol dehydrogenase gene, allowing the further development of aroma and participates in the control of berry acidity (Chervin et al. 2004, Tesniere et al. 2004). Some A. thaliana mutants affected in the perception (Zhou et al. 1998) or the transduction of ethylene, are hypersensitive to sugars, pointing to the existence of negative interactions between both signal transduction pathways (Gibson et al. 2001, Leclercq et al. 2002, Yanagisawa et al. 2003).

In tomato, the ripening-inhibitor (rin) mutation impairs the typical ripening-associated increase in ethylene production that occurs during climacteric fruit maturation and the fruit does not ripen. The mutation affects a gene encoding for a MADS-box transcription factor. Such proteins are widespread in all eukaryotic kingdoms and involved in growth and developmental processes. In plants, they were first characterized in the context of floral initiation and meristem differentiation, and recently implicated in developmental, non-hormonal control of fruit ripening (Vrebalov et al. 2002, Giovannoni 2004). In grape, although many genes encoding MADS-box proteins are expressed in flower, some are found in the fruit: VvMADS5 is expressed during early berry development while VvMADS1 and VvMADS4 expression is strong throughout development (Boss et al. 2001, 2002, 2003, Chatelet et al. 2007). However, there is no information available about its putative involvement in ethylene signalling.

Processes like the accumulation of sugars, the metabolism of organic acids, the synthesis of aroma compounds and the accumulation of anthoyanins in the skin of grape appear to be controlled by brassinosteroids (BRs; Symons et al. 2006). The role of these hormones in both climacteric and non-climacteric fruits ripening processes is also evidenced. Indeed, application of these compounds promotes tomato fruit and grape berry ripening, increases sugar levels and decreases acid contents in both species. They also enhance the accumulation of lycopene in the pericarp of tomato fruit and of anthocyanins in grape berry (McMorris 1997, Vidya Vardhini and Rao 2002, Symons et al. 2006, Pi-lati et al. 2007). In tomato however, their effect on fruit ripening could be indirect, through the increase of ethylene levels (Vidya Vardhini and Rao 2002). In grape, there is a dramatic increase of some BRs at the onset of ripening (Sy-mons et al. 2006).

The characterization of pleiotropic mutations also provides clues regarding the complexity of inter-connections of sugars, hormonal and environmental trans-duction pathways. Besides being involved in sugar signalling, the prl1 (Nemeth et al. 1998), gin2 (Moore et al. 2003), ctr1 (Gibson et al. 2001, Leclercq et al. 2002) and bls1 (Laxmi et al. 2004) mutations are also implicated in hormonal and environmental responses. The discovery that a SNF1-Related kinase complex is also differentially regulated by ABA and GAs provides strong evidence for a link between hormonal and sugar-sensing pathways controlling seed development, dormancy, and germination in tomato (Bradford et al. 2003).

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