JXB Advance Access originally published online on June 18, 2004
Journal of Experimental Botany 2004 55(404):1871-1879; doi:10.1093/jxb/erh184
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RESEARCH PAPER |
Post-genomics approaches for the elucidation of plant adaptive mechanisms to sulphur deficiency
Department of Molecular Biology and Biotechnology, Graduate School of Pharmaceutical Sciences, Chiba University, CREST of JST (Japan Science and Technology Agency), Yayoi-cho 1-33, Inage-ku, Chiba 263-8522, Japan
* To whom correspondence should be addressed. Fax: +81 43 290 2905. E-mail: ksaito{at}faculty.chiba.u.jp
Received 4 February 2004; Accepted 23 April 2004
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Abstract |
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 Top Abstract IntroductionEarly studyExperimental design for...Global change in transcriptomeFunctional analysis of -S...ConclusionsReferences |
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With the genome sequence of Arabidopsis and rice now available, plant science has stepped forward into a new phase. Post-genomics studies such as transcriptomics, proteomics, and metabolomics will bring about a breakthrough for the functional elucidation of genes and for an understanding of a whole process of living cells. Concerning studies of sulphur (S) metabolism, several reports have recently been published describing the transcript profiles of S-starved Arabidopsis. In this review, these -omics studies that have revealed the network linking several pathways related to jasmonic acid (JA), oxidative stress response, auxin, and flavonoid to S metabolic pathway are summarized.
Key words: Adaptive response, Arabidopsis, DNA array, global, metabolomics, network, O-acetyl-L-serine, sulphur deficiency, transcriptomics
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Introduction |
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TopAbstractIntroductionEarly studyExperimental design for...Global change in transcriptomeFunctional analysis of -S...ConclusionsReferences |
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Sulphur deficiency (–S) results in decreased crop yields and quality. From an agricultural point of view, the symptoms and responses of plants subjected to –S have been extensively reported by studies in plant physiology (Crawford et al., 2000
). S-starved plants exhibit stunted growth and chlorosis, and sometimes turn reddish. The ratio of root biomass to that of the above-ground part increases. The contents of sulphate and S-containing compounds such as cysteine, methionine, and glutathione (GSH) decrease. Protein synthesis is repressed and hence the contents of the soluble nitrogen pools such as nitrate and amides increase. The S storage pool is remobilized. The amount of S-rich seed-storage proteins decreases, whereas that of S-poor seed-storage proteins increases to compensate for the reduction of total proteins in seeds. The activities of sulphate uptake and assimilation are derepressed. The addition of O-acetyl-L-serine (OAS), a precursor of cysteine biosynthesis, also enhances sulphate uptake and assimilation activity, suggesting that OAS plays a role both as a substrate for organic S-compound biosynthesis and as a regulator of S metabolism (Saito, 2000). S deficiency is considered as a sulphur shortage relative to nitrogen (N) nutrition, because several responses under –S, such as changes in seed storage protein composition, diminish when N supply is limited simultaneously.
Since 2000, plant science has moved forward into the stage of post-genomics. The first transcriptome analysis of a plant using a DNA array was reported (Wang et al., 2000) and sequencing of the Arabidopsis (Arabidopsis Genome Initiative, 2000) and rice (Yu et al., 2002; Goff et al., 2002) genomes were completed. Recently, -omics studies, in particular transcriptome analyses of S-starved Arabidopsis were reported elucidating a whole molecular mechanism of various responses to –S (Hirai et al., 2003a, b; Maruyama-Nakashita et al., 2003; Nikiforova et al., 2003; Saito, 2003). In this review, the results of these recent -omics studies are summarized, and –S-adaptive responses are discussed with regard to the regulation of gene expression.
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Early study |
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TopAbstractIntroductionEarly studyExperimental design for...Global change in transcriptomeFunctional analysis of -S...ConclusionsReferences |
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In the era of classical molecular biology and genetics, molecular mechanisms of the responses to –S have been partially clarified. The gene encoding the ß subunit of ß-conglycinin, a S-poor seed-storage protein of soybean, is one of the earliest –S-inducible genes of those that have been cloned from plants (Tierney et al., 1987
). Using transgenic plants, changes in accumulation of the ß subunit in soybean seeds in response to S nutrition were shown to be regulated at the level of transcription driven by the ß subunit promoter (Fujiwara et al., 1992; Hirai et al., 1994, 1995; Naito et al., 1994, 1995). Genes encoding sulphate transporters and S-assimilatory enzymes have been cloned from plants since 1992 (Saito et al., 1992; Smith et al., 1995), and since then it has been shown that several genes in the S-uptake and assimilation pathways are up-regulated at the transcriptional level under –S (Takahashi et al., 1997; for reviews see Hawkesford, 2000; Leustek et al., 2000; Saito, 2000). OAS was proved to be a positive regulator of gene expression encoding sulphate transporters and assimilatory enzymes in plant (for reviews see Hawkesford, 2000; Leustek et al., 2000; Saito, 2000). The OAS content in plant organs is regulated by both S and N nutrition; it increases under –S and decreases under –N (Kim et al., 1999). Transcriptional activity of the soybean ß subunit gene promoter, in parallel with OAS content, increased as the S/N ratio in the plant-culture media decreased, suggesting that OAS is a candidate for regulating the co-ordination of S and N nutrition at a transcriptional level (Kim et al., 1999; Hirai et al., 2002). The molecular mechanism for the involvement of OAS in such transcriptional regulation still remains to be clarified: either direct involvement of OAS binding to a particular trans-acting factor as established in a bacterial system (Kredich, 1993), or an indirect connection, probably via metabolic consequence (Hawkesford et al., 2003). Genetic studies have also revealed pathways and regulation of S metabolism (for reviews see Hawkesford, 2000; Leustek et al., 2000; Saito, 2000). Using Arabidopsis, several groups made an effort to isolate mutants which have defects in the S-metabolic pathway or the signal-transduction pathway involved in –S response. By the isolation of mutants resistant to selenate, a toxic analogue of sulphate, Sultr1;2, was identified as a transporter responsible for the import of sulphate from the environment into the roots (Shibagaki et al., 2002; Yoshimoto et al., 2002). However, the isolation of mutants having defects in the –S response (Fujiwara et al., 1997) was difficult, probably because the plant has a redundant system to cope with –S stress. |
Experimental design for transcriptomics and metabolomics |
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TopAbstractIntroductionEarly studyExperimental design for...Global change in transcriptomeFunctional analysis of -S...ConclusionsReferences |
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In the papers describing the transcriptome under –S (Hirai et al., 2003a
, b; Maruyama-Nakashita et al., 2003; Nikiforova et al., 2003), Arabidopsis were grown on sterile agarose-solidified media in plates (Table 1). Wild-type plants were grown under continuous –S conditions, or the plants grown under +S control condition were transferred to –S or OAS-supplemented media. Maruyama-Nakashita et al. (2003) also used sel1-10, a knockout mutant of Sultr1;2. Wild-type Arabidopsis was also grown by hydroponic culture under continuous –S, –nitrate (–N), and –SN conditions for 3 weeks (Hirai et al., 2004). Leaves, roots or whole seedlings were analysed for transcript profiles by DNA macro- or microarray (Table 1). The metabolome of leaf and root samples was also analysed by using Fourier-transform ion cyclotron MS (FT-MS), HPLC, and capillary electrophoresis (CE).
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S-nutrient status in plants varied depending upon the sulphate concentration in the culture media, plant-growth stage, period under –S condition, and plant density in the culture media. In the study by Nikiforova et al. (2003)
, seedlings were sampled just before (Exp 1.1 and 2.1), and after (Exp 1.2 and 2.2) the onset of visible symptoms of –S such as retarded growth and chlorosis. The total content of elemental S in S-starved plants decreased from 43% to 27% of that in control plants, and GSH content dropped by 7–15-fold. Cys was reduced to non-measurable levels in all four experiments. OAS, Ser and Trp levels in S-starved plants increased by 5–37-fold, 2–3-fold, and 6–28-fold compared with control plants, respectively. Their growth conditions mimicked long-term S starvation and the degree of S shortage was relatively more severe than that in the other studies. In the study by Hirai et al. (2003a, b), to elucidate the early response to –S, plants did not show any visible symptom for at least 1 week after transfer. At the time, when plants were sampled for analysis (48 h after transfer), the sulphate content in the S-starved plants decreased by 4-fold and 2-fold in leaves and roots, respectively. GSH content decreased by 2-fold only in S-starved leaves, whereas Cys content did not change significantly in both S-starved leaves and roots. The OAS content in S-starved plants increased by 2.4-fold and 4.7-fold in leaves and roots, respectively. Plants subjected to continuous nutrient starvation also did not show any visible symptoms (Hirai et al., 2004). In the study by Maruyama-Nakashita et al. (2003), the sulphate content in roots decreased by 2-fold (HL compared with HH, shown in Table 1), decreased by 4.3-fold (LL compared with HH), and increased by 4.4-fold (LH compared with LL). The growth of sel1-10 mutants was significantly retarded compared with wild-type plants even though plants were grown under +S condition. In the sel1-10 mutants, the sulphate content both in the leaves and roots decreased to 20% compared with wild-type plants regardless of Sultr1;1 induction, suggesting that SULTR1;2 functions as a major component of the initial sulphate uptake system in Arabidopsis roots. In their shift experiments, plants were harvested 24 h after transfer. In the experiment using a knockout mutant, it was suggested that dysfunction of SULTR1;2 mimicked –S. |
Global change in transcriptome |
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TopAbstractIntroductionEarly studyExperimental design for...Global change in transcriptomeFunctional analysis of -S...ConclusionsReferences |
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Generally, array experiments produce a huge amount of data in multi-dimensional space; in the authors' case (Hirai et al., 2003a
, b, 2004), data were expressed in 13 000 ESTs x14 samples (see Table 1) matrix. To understand global transcript profiles, simplification and visualization of data are indispensable. The simplest way to plot expression data is in a two-dimensional scatter plot and to calculate the correlation coefficients of all one-to-one combinations of experiments.
Figure 1 shows scatter plots of Fold Change value, i.e. the ratio of the average signal intensities in the treated sample to those in the appropriate control sample. Several aspects of global transcriptome were elucidated from these one-to-one comparisons. In Fig. 1A, Fold Changes in roots by 48 h S starvation (P-ro-S) were plotted against those by 48 h OAS treatment (P-ro-O). There was a positive correlation between the Fold Change by sulphur deficiency and that by the OAS treatment (R2=0.42 for root; 0.30 for leaf, data not shown). This suggests that OAS treatment mimicked short-term (48 h) –S treatment and that OAS is one of the positive regulators of not only specific gene expression, such as sulphate transporters, APS reductases (APR), and soybean ß subunit of ß-conglycinin, but also global transcriptome under –S (Hirai et al., 2003a, b). In Fig. 1B, Fold Changes by continuous 3-week S starvation in leaves (H-le-S) were plotted against those in roots (H-ro-S). Apparently, there was no significant correlation between the Fold Changes in leaves and roots. This indicated that the set of genes induced or repressed by continuous 3-week S starvation in leaves was different from that in roots. It was also the case with leaves and roots subjected to 48 h S starvation (P-le-S versus P-ro-S; Hirai et al., 2003a). In a similar way, Fig. 1C showed that the set of genes induced or repressed in leaves subjected to continuous 3-week S starvation (H-le-S) was different from that of 48 h S starvation (P-le-S). It was also the case with roots (H-ro-S versus P-ro-S; data not shown).
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Global metabolic profiles can be analysed in the same way as the transcript profiles shown above. Interestingly, similar trends as those shown in Fig. 1 were also observed in the metabolome (Fig. 2).
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As other ways to simplify and visualize complicated data and classify genes or treatments according to expression pattern, hierarchical clustering analysis (HCA), principal component analysis (PCA), and self-organizing map (SOM) analysis are used. BL-SOM (batch-learning SOM; Kanaya et al., 2001
; Abe et al., 2003) is being used successfully to classify genes and metabolites measured by metabolome analysis (Hirai et al., 2004). |
Functional analysis of –S-responsive genes |
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TopAbstractIntroductionEarly studyExperimental design for...Global change in transcriptomeFunctional analysis of -S...ConclusionsReferences |
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Through those studies, –S-responsive genes were noted based on the following criteria. Hirai et al. (2003a
, b) conducted statistical analysis SAM (Significance Analysis of Microarrays; Tusher et al., 2001) using data obtained from repetitive hybridizations, and selected the genes exhibiting statistically significant up- or down-regulation. Nikiforova et al. (2003) also conducted repetitive hybridizations and picked up the clones whose fold change was greater than 2.5 or less than 0.4 with P<0.05 by t-test in at least one of the four experiments (in the case for transcriptional factors, a fold change greater than two or less than 0.5 with P<0.05). The clones regulated not only by –S, but also by other stresses (–Fe, +herbicides), were eliminated. In the study by Maruyama-Nakashita et al. (2003), the genes exhibiting greater than a 2-fold change in three comparisons of HL versus HH, LL versus HH, and KO-R versus Ws-R, and exhibiting less than a 0.5-fold change compared with LH versus HH were selected. The genes exhibiting less than a 0.5-fold change values in three comparisons of HL versus HH, LL versus HH, and KO-R versus Ws-R, and exhibiting greater than a 2-fold change compared with LH versus HH, were also selected.
By combining these results, networks of several pathways under –S were clearly drawn, in addition to the S uptake and the assimilation pathways as expected. In the authors' experiments using plants subjected to 48 h S starvation, changes in the jasmonic acid pathway were most notable. Several JA-biosynthetic genes were up-regulated and known JA-responsive genes were also regulated (Fig. 3A), suggesting that the JA level in the plant, especially in leaves, actually increased under –S (Hirai et al., 2003a). Interestingly, the –S-responsive APR1 gene was induced by JA treatment (Sasaki-Sekimoto et al., 2003). Cross-talk between the S assimilation pathway and the JA pathway is suggested.
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The expression of the genes involved in glucosinolate (GLS) biosynthesis and degradation changed (Fig. 3A). CYP83A1, one of the genes responsible for aldoxime oxidation, showed statistically significant down-regulation in both P-le-S and P-ro-S (SAM; False Discovery Rate <10 %). CYP79F1 and CYP79B3, which are responsible for aldoxime formation, were down-regulated in P-le-S and P-ro-S, respectively. The MAM-1 gene involved in the side-chain elongation of methionine, one of the precursors of GLSs, was down-regulated in P-le-S. Expression of the two genes (At1g52000 and At5g25980) encoding myrosinase, a GLS degrading enzyme, was repressed in P-ro-S. Metabolome analysis by FT-MS showed decreased GLSs accumulation in P-le-S and P-ro-S. Under continuous 3-week –S, –N, and –SN conditions, genes involved in this pathway were regulated in a treatment-specific manner (Hirai et al., 2004
; Fig. 3B). Metabolome analysis showed that the accumulation pattern of GLSs changed according to the changes in gene expression. The results also suggested that GLS accumulation pattern is determined by the two roles of GLSs, as a S storage source and as a defence compound to pathogen and herbivore attack (Hirai et al., 2004).
In the study by Nikiforova et al. (2003), down-regulation of genes involved in electron transport and membrane-associated energy conversion was notable. The SQD2 gene, responsible for sulpholipid biosynthesis, was also down-regulated. On the other hand, genes involved in several pathways were significantly up-regulated: genes involved in the GSH redox cycle, a homologue of the isoflavonoid reductase gene (At1g75280), aromatic amino acid biosynthetic genes, genes suggested to be involved in the activation of flavonoid biosynthesis (R2R3-MYB transcription factors) and flavonoid accumulation (glutathione transferases), genes involved in auxin biosynthesis (including myrosinase and nitrilase), auxin-responsive genes, and JA biosynthetic genes were up-regulated. From these results, Nikiforova et al. (2003) speculated the following schema. Under –S, a reduction of photosynthesis capacity caused by the decrease of sulpholipid results in high-light stress as oxidative stress. The content of GSH, which plays a role as a scavenger of active oxygen species, decreases due to S shortage and hence anthocyanin accumulates as an alternative way to protect against high-light stress. Over-accumulation of tryptophan and degradation of indoleGLS by myrosinase and nitrilase led to auxin (indole-3-acetate) accumulation, which triggers induced root growth (Fig. 3B). The nitrilase 3 gene is induced under –S and may be involved in auxin production under –S (Kuts et al., 2002). In the authors' experiments, using plants in which GSH content did not decrease drastically, the oxidative stress-response pathway and flavonoid pathway did not show notable change.
Maruyama-Nakashita et al. (2003) found that genes involved in secondary sulphur metabolism (CYP79B3, a sulphotransferase gene, a putative thiamine biosynthetic gene, and a metallothionein-like gene) were down-regulated in roots, suggesting that the consumption of a sulphur source can be minimized by the modification of metabolic fluxes in secondary S metabolism. On the other hand, a set of genes related to the oxidative stress response (a Met sulphoxide reductase gene, HSP21 gene, a homologue of isoflavone reductase gene (At1g75280) and a carbonic anhydrase gene), and a JA biosynthetic gene were up-regulated in roots, probably due to the decrease of GSH content. Two putative thioglucosidase genes (At2g44460 and At3g60140), which may act for GLS degradation, were also up-regulated. These results again suggested a close connection of GLS metabolism to S nutrition as indicated by Hirai et al. (2003a).
Table 2 shows –S-responsive genes that were identified as genes up- or down-regulated by –S in at least two out of the four studies above. Combining this gene list and the other results obtained from the above studies, a tentative model of –S response is illustrated in Fig. 3. The JA pathway and the GLS pathway were modulated from a relatively early time after transfer to –S. JA signalling is possibly involved in the relatively short-term –S responses, especially in leaves (Hirai et al., 2003a, b). GLS accumulation may be repressed to save S for primary metabolism. Putative thioglucosidases (At2g44460 and At3g60140) and a myrosinase-associated protein (At3g14210) may be involved in GLS degradation. Auxin (indole-3-acetate) biosynthesis through indoleGLS seemed to be induced mainly in roots as a relatively long-term response to –S. It is consistent with the putative role of auxin as a trigger of root growth under –S. Actually, regulation is more complicated than the summary in Fig. 3. Cross-talk among the JA signalling pathway, the auxin signalling pathway and GLS metabolism must exist within and between organs.
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No identical transcriptional factor is identified as common in more than two studies. One reason is that each array used in these studies contained only approximately one-third of all Arabidopsis genes. The expression level of the transcription factor is expected to be low and the ESTs of the transcription factor were not always available for the preparation of the array. Alternatively, in these studies, final physiological responses varied depending on the severeness of S shortage, the plant-growth stage, and the period of –S stress; that is, the most downstream genes in the signal-transduction pathway were different from experiment to experiment. Hence it is reasonable that different transcriptional factors were regulated in these experiments. Analysis of the one-to-one correlation between all combinations of two genes will help to identify the specific transcription factor for a specific response.
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Conclusions |
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TopAbstractIntroductionEarly studyExperimental design for...Global change in transcriptomeFunctional analysis of -S...ConclusionsReferences |
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Microarrays carrying almost all the Arabidopsis genes have recently become available. By transcriptomics, the molecular mechanism of physiological changes under –S, known for a long time in fields, will be outlined. As the functions of about a half of the Arabidopsis genes are still not experimentally determined, a classical molecular biological and genetic approach, together with a post-genomics approach, are needed to clarify the molecular mechanism underlying the response to nutritional stress combined with gene function. Since the gene expression pattern is regulated by a metabolite accumulation pattern and vice versa, metabolomics is also indispensable for an understanding of the whole mechanism.
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Acknowledgements |
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This research was supported in part by CREST to JST, and by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology, Japan.
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