Annals of Botany 89: 803-811, 2002
© 2002 Annals of Botany Company
Classification of Genes Differentially Expressed during Water-deficit Stress in Arabidopsis thaliana: an Analysis using Microarray and Differential Expression Data
1Department of Botany and Plant Sciences, and The Center for Plant Cell Biology, University of California, Riverside, CA 92521, USA
* For correspondence. E-mail elizabeth.bary{at}ucr.edu
Received: 25 June 2001; Returned for revision: 11 September 2001; Accepted: 11 February 2002.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONGENES REGULATED BY WATER-DEFICIT...PREDICTED FUNCTIONS OF...FUNCTION OF DOWN-REGULATED GENESCONCLUSIONSLITERATURE CITED |
|---|
Many changes in gene expression occur in response to water-deficit stress. A challenge is to determine which changes support plant adaptation to conditions of reduced soil water content and which occur in response to lesions in metabolic and cellular functions. Microarray methods are being employed to catalogue all of the changes in gene expression that occur in response to specific water-deficit conditions. Although these methods do not measure the amount or activities of specific proteins that function in the water-deficit response, they do target specific biochemical and cellular events that should be detailed in further work. Potential functions of approx. 130 genes of Arabidopsis thaliana that have been shown to be up-regulated are tabulated here. These point to signalling events, detoxification and other functions involved in the cellular response to water-deficit stress. As microarray techniques are refined, plant stress biologists will be able to characterize changes in gene expression within the whole genome in specific organs and tissues subjected to different levels of water-deficit stress.
Key words: Water-deficit stress, gene expression, Arabidopsis thaliana.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONGENES REGULATED BY WATER-DEFICIT...PREDICTED FUNCTIONS OF...FUNCTION OF DOWN-REGULATED GENESCONCLUSIONSLITERATURE CITED |
|---|
Plant cellular water-deficit stress may occur under conditions of reduced soil water content. Under these conditions, changes in gene expression take place, with up- as well as down-regulation occurring. The changes in gene expression may be regulated directly by the stress conditions or may result from secondary stresses and/or injury responses (Hanson and Hitz, 1982). Changes in gene expression are induced by a complex series of signal transduction events that have not been clearly delineated. One of the signals involved is abscisic acid (ABA), although there are clearly other signal molecules that have not yet been identified. Signals that result in changes in gene expression may result from an injury response and/or may be responsible for inducing genes that may have an adaptive function.
The function of gene products that have altered abundance during water-deficit stress may be defined by the ability of the gene product to promote water-deficit stress survival. Some gene products may be involved in promoting stress tolerance and some may not. Those that are not may be expressed as a result of injury such as a block in metabolism. One of the important challenges is to understand which genes function to promote cellular and whole plant tolerance of water-deficit stress.
Gene expression patterns are influenced by the severity, extent and rate or application of the stress (Bray et al., 2000). Gene expression patterns may be altered at the initial step—increasing the transcription rate of a specific gene—or at subsequent steps that control specific mRNA levels or the translation of a specific mRNA. Together a complex pattern of gene expression is established that is a result of the specific stress conditions. Hanson and Hitz (1982) argued that when stress is imposed rapidly a greater number of responses will be injury-induced than under a slower long-term application of water-deficit stress.
|
GENES REGULATED BY WATER-DEFICIT STRESS |
|---|
|
TOPABSTRACTINTRODUCTIONGENES REGULATED BY WATER-DEFICIT...PREDICTED FUNCTIONS OF...FUNCTION OF DOWN-REGULATED GENESCONCLUSIONSLITERATURE CITED |
|---|
Microarray analyses provide a powerful method to study the many changes in gene expression that occur in an organism in response to developmental and environmental cues. For water-deficit stress, microarray analyses using full-length cDNAs obtained from Arabidopsis thaliana plants subjected to different stresses have been published (Seki et al., 2001). To identify changes in expression patterns in response to water-deficit stress, Seki et al. (2001) dehydrated 3-week-old Arabidopsis thaliana plants on filter paper (60 % RH, 22 °C) for 2 h (Yamaguchi-Shinozaki and Shinozaki, 1994). From an array containing 1300 full-length cDNAs isolated from libraries prepared from stressed plants, 44 genes were confirmed to be induced by the water-deficit treatment after RNA blot analyses (Table 1; Seki et al., 2001). Sixty-eight per cent had not been previously identified as water-deficit-induced genes. A microarray study, using arrays originally designed for studies in wound induction of gene expression, on water-deficit gene induction using a similar method of stress imposition was also published (Reymond et al., 2000; supplemental information at http://www.unil.ch/ibpv/docs/WWWPR/Docs/listegenes.html). This resulted in the identification of further genes that are up-regulated at the mRNA level (Table 1). The experiments completed thus far have involved a severe, rapid stress and were not completed with microarrays that contain the whole genome. Even though the stress imposed in these two studies was rapid and severe, it is still worthwhile evaluating the patterns of gene expression that are altered, and comparing these changes with what is know about alterations in metabolism. In addition to genes identified by these arrays, genes identified using standard differential expression methods have been compiled for this analysis of water-deficit alterations in gene expression.
|
|
PREDICTED FUNCTIONS OF ARABIDOPSIS GENE PRODUCTS |
|---|
|
TOPABSTRACTINTRODUCTIONGENES REGULATED BY WATER-DEFICIT...PREDICTED FUNCTIONS OF...FUNCTION OF DOWN-REGULATED GENESCONCLUSIONSLITERATURE CITED |
|---|
A system to categorize gene function has been applied to known plant and animal genomes. Genes are broken down into at least 13 general categories (http://mips.gsf.de/proj/thal/db/tables/tables_func_frame.html). In the Arabidopsis thaliana genome, the largest category is that of unclassified, or genes whose function has not been determined (Arabidopsis Genome Initiative, 2000). Many genes involved in water-deficit stress also fall into this category. Some, such as the LEA (late embryogenesis abundant) proteins, have been much studied, yet their function remains unknown (Garay-Arroyo et al., 2000). Others are completely unknown in that an mRNA (or EST) has not been previously identified and there is no amino acid sequence homology with other proteins of known function. The categories include one called ‘cell rescue, defence, cell death and ageing’. Many of the genes known to be induced by water deficit are placed in this category even though an exact function is not understood. Instead of using this category, the present analysis places genes into a potential functional category or into the unclassified category, if the function is not known. In Table 1, it is noted if these genes are targeted to a specific cellular compartment or if they contain predicted transmembrane domains. Genes induced by water-deficit stress have been allocated to 11 different functional categories (Table 1; Fig. 1). Since a whole genome analysis of the genes expressed in response to water-deficit stress has not yet been published, the categories and conclusions drawn are only preliminary. More genes will almost certainly be identified as further microarray analyses are completed, and more information will be gained about gene expression and function as different techniques for stress imposition are used.
|
In addition to the functional categories of proteins established at MIPS (Münich Information Centre for Protein Sequences), it is also appropriate to consider whether the potential function of a gene product has an adaptive role in water-deficit stress. Induction of gene expression does not necessarily imply that a gene will play an adaptive role. Depending upon the conditions to which the plant was subjected, some of genes that are expressed may indicate that the plant has been subjected to an injury and/or a secondary stress. For example, 11·4 % of the genes in Table 1 are likely to be involved in detoxification of oxidative stress. It is uncertain whether these genes are induced directly by cellular water deficit or by the resulting oxidative stress. The increased production of ROS (reactive oxygen species) may arise from the reduced CO2 available for photosynthesis causing a decrease in re-oxidation relative to reduction (Smirnoff, 1993; Asada, 1999). This may lead to the generation of O2*– and H2O2. Therefore, the signals that induce the genes may also provide valuable insight into gene function.
It must also be considered whether cellular functions can be inferred from RNA expression levels. Of course, mRNA accumulation is not the only level of gene expression that is regulated. It can be argued that both protein accumulation and activation should be the targets of gene expression studies. Therefore, studies at the mRNA level should be used to target particular processes for further study. Water-deficit studies have already documented an increase in mRNA content when there is no increase in protein content. For example, an aquaporin RD28 is induced at the mRNA level (Yamaguchi-Shinozaki et al., 1992) but when the protein levels were studied no change in protein content was observed in response to different levels of water deficit (Daniels et al., 1994). Also, the gene ERD1, which encodes a ClpC-like ATPase that may interact with chloroplast-localized ClpP protease, is induced by stress and senescence at the mRNA level, but the protein levels declined with senescence (Weaver et al., 1999).
Metabolism
It has been known for some time that cellular metabolism is altered by water-deficit stress (Hsiao, 1973); however, detailed analyses on the effect of stress on the majority of the enzymes in individual metabolic pathways is lacking. Of changes that are known, it remains unclear which are brought about as an adaptive response and which represent lesions in metabolic pathways. Most work has concentrated in the areas of photosynthesis (carbon and energy metabolism; reviewed by Chaves, 1991), carbon and nitrogen utilization (Foyer et al., 1998), and the synthesis of small molecules that potentially play a role in osmotic adjustment (reviewed by Bray et al., 2000). The activities of a number of enzymes have been demonstrated to increase or decrease in response to water deficit (reviewed by Todd, 1972). It is generally unknown if these are regulated at the level of enzyme activity or through alterations in the transcription and translation of specific genes. A portion of these changes can be substantiated by known changes in gene expression at the mRNA level. The genes identified in the two microarray studies that fall into the metabolism category are largely involved in three main processes: amino acid, phenylpropanoid and fatty acid metabolism (Table 1). The majority of these were identified on the wound microarray, which is heavily biased towards genes known to be regulated in a defence response. Nitrate reductase activity has been shown to be decreased by water-deficit stress in a number of species (e.g. Foyer et al., 1998). This gene was also strongly down-regulated at the mRNA level in arabidopsis (http://www.unil.ch/ibpv/docs/WWWPR/Docs/listegenes.html).
Energy
It is well documented that photosynthetic carbon and energy metabolism is decreased by water-deficit stress (Chaves, 1991). Considerable discussion continues over the mechanism for the decrease. It has been demonstrated that there is a decrease in the mRNA that encodes the small subunit of Rubisco (Bartholomew et al., 1991). In tomato plants subjected to water-deficit stress the mRNA is decreased through inhibition of transcription (Cohen et al., 1999). In addition, dark respiration is decreased (Hsiao, 1973). The microarrays only note two genes of central energy metabolism that are up-regulated in response to water-deficit stress.
Transcription
Transcription factors are required to regulate changes in gene expression in response to water-deficit stress. The Arabidopsis thaliana genome contains more than 1500 transcription factors, many of which are specific to plants (Riechmann et al., 2000). Several different classes of transcription factors are induced by water-deficit stress (Table 1), including bZIP (AREB1), homeodomain (ATHB-6, –7 and –12), AP2 domain (DREB2A), MYB (ATMYB2) and MYC-related factors. These are all likely to be involved in the up-regulation of genes, many of which are signalled through ABA. A gene encoding a transcription factor involved in the ethylene response is induced as well as a 14-3-3 like protein (Reymond et al., 2000). Many of these transcription factors are members of large multigene families. It will be important to determine if some members have a role as repressors prior to water-deficit stress. Mutant studies will allow questions to be asked about other responses that are controlled by these transcription factors.
A stress-induced histone H1 was also identified (Ascenzi and Gantt, 1999). This is similar to a stress-induced histone H1, H1-S, identified in tomato and its relatives (Scippa et al., 2000). This histone may play a role in maintaining chromatin structure during water deficit.
Protein destination
Many genes that are induced are involved in the fate of proteins that have been synthesized. Water deficit may cause proteins to become aggregated or malformed which may either require protein degradation or chaperone activity. Accordingly, some mRNAs of genes that encode proteases and chaperones are induced. However, the proteases induced are cysteine proteases and metallopeptidases that are predicted to reside in the vacuole (or the cell wall) rather than in the cytoplasm. Protease inhibitors are also induced which may indicate that a balancing mechanism is also required. There are a number of likely roles for the cysteine proteases and metallopeptidases that have increased mRNA levels in tissues responding to water-deficit stress. First, cysteine proteases have been shown to be induced by oxidative stress in soybean cells, and to play a role in programmed cell death (Solomon et al., 1999). Since other genes involved in oxidative stress are induced in arabidopsis, it is possible that these cysteine protease genes are induced by the oxidative stress that accompanies water deficit and may be a harbinger of cell death. Secondly, they may be important for breakdown of stored proteins to be used when the stress is relieved as a source of free amino acids for increased protein synthesis (Vierstra, 1996). It is also possible that the degraded proteins are transported into the vacuole during stress, although a mechanism for this has not been established (Vierstra, 1996). Thirdly, once a cell has been lysed, these types of proteases might also be involved in defence of cells that have not been damaged.
Transport
The only genes induced in the transport category in response to water-deficit stress are involved in water transport and sugar transport. Aquaporin mRNAs are increased in response to water deficit, yet, as mentioned above, interpretation of these results should be undertaken with caution as protein levels were not found to increase in response to water deficit in one study (Daniels et al., 1994). Three of the 23-plus aquaporins (Weig et al., 1997) that have been identified in the Arabidopsis thaliana genome are known to be induced by water-deficit stress at the mRNA level. Two are predicted to function in the plasma membrane and one in the tonoplast. For these proteins, the programme used at MIPS to predict transmembrane domains may underestimate the number of domains. Only four or five transmembrane domains (Table 1) are predicted when all models of aquaporins indicate six transmembrane domains. The tissues and organs in which the genes are expressed will play an important role in the function of these genes (Hsiao and Xu, 2000). Although protein levels do not increase in whole organs, when specific cell types are evaluated there may be a change in protein content and activity. It is important to identify the specific cells of expression since increased expression in all cell types could increase water loss because water movement through aquaporins is dependent upon the water potential gradient. A potential sugar transport gene has also been shown to be up-regulated by water-deficit stress, yet genes involved in ion transport have not been identified in microarrays or in other gene expression studies.
Cell communication/signal transduction
In the microarrays, few potential signalling molecules were identified. Is this because the mRNA levels were not altered, were not very abundant or cDNAs were not included in the array? However, many genes have been identified that play a potential role in the regulation of cellular processes in response to water-deficit stress (Table 1). The Shinozaki/Yamaguchi-Shinozaki groups in Japan identified many of these genes in stress libraries. These implicate MAP kinase cascades as well as phosphatidylinositide signalling pathways. In addition, these genes provide impetus to further study the role of calcium in the regulation of the water-deficit response.
Cell rescue, defence, cell death and ageing
A number of genes that may be classified in the cell rescue or defence category are up-regulated in response to water-deficit stress. The two largest groups identified thus far are in the amelioration of oxidative stress and/or in defence against pathogens. Increased expression of antioxidant enzymes, including ascorbate peroxidase, glutathione reductase, catalase and superoxide dismutase (Jagtap and Bhargava, 1995; Sairam and Saxena, 2000; Borsani et al., 2001) correlate with increased stress resistance. The mRNAs corresponding to these genes are induced by water deficit. The genes involved in phenylpropanoid metabolism categorized under metabolism also have a potential role as antioxidants. Phenolics and phenylpropanoids have free radical trapping properties.
Cellular organization
Cell wall function and characteristics may also be changed in response to cellular water-deficit stress (Wu and Cosgrove, 2000). Growth as described by the Lockhart equation (Lockhart, 1965) measures a relative rate of irreversible volume increase as the product of volumetric extensibility (m) and the difference between turgor pressure (
p) and the yield threshold turgor pressure (Y).
dV/V·dt = m (p – Y)
Therefore, growth of a cell will only occur when turgor pressure is greater than a minimum threshold. Water stress may decrease growth through a decrease in turgor. However, this may be compensated by changes in both m and Y, which are measures of the plasticity of the cell wall (Hsiao and Xu, 2000). For growth to continue under reduced turgor, cell wall extensibility may be increased or the yield threshold decreased, making cell expansion possible under conditions of reduced turgor. In addition, cell wall shrinkage with water loss will reduce the loss of cell turgor (Tyree and Jarvis, 1982). In a study on jack pine roots subjected to PEG treatment, cell walls were shown to constrict around the shrinking protoplast which served to maintain turgor pressure (Marshall and Dumbroff, 1999). It is argued that new proteins accumulating in the cell wall played a role in the alterations in cell wall elasticity that occurred throughout the stress period. A number of genes induced by water deficit may be predicted to play a role in altering the characteristics of the cell wall. These include a polygalacturonase-like gene product and a polygalacturonase inhibitor. A ß-glucosidase and a gene product with pectinesterase activity may also be involved in altering the extracellular matrix. Other gene products that may be secreted into the cell wall to alter cell wall properties have not been identified in Arabidopsis thaliana. Although studies have shown that proteins accumulate in cell walls in response to water-deficit stress (Bozarth et al., 1987; García-Gómez et al., 2000), the function of these proteins has not been identified. The proline-rich proteins identified in bean cell walls subjected to water-deficit stress were shown to interact with a membrane protein.
Uncharacterized/classification not yet clear cut
Notably, the hydrophilic proteins that have been called LEA proteins remain a very interesting group. These proteins have been classified into several different groups based on amino acid sequence (Bray et al., 2000). New work continues to uncover the important role of these proteins in the dehydrating cytoplasm (Wolkers et al., 2001). The different characteristics predicted from the protein structure indicate that the proteins may play distinct roles in cells subjected to water-deficit stress, although the molecular function remains unclear.
|
FUNCTION OF DOWN-REGULATED GENES |
|---|
|
TOPABSTRACTINTRODUCTIONGENES REGULATED BY WATER-DEFICIT...PREDICTED FUNCTIONS OF...FUNCTION OF DOWN-REGULATED GENESCONCLUSIONSLITERATURE CITED |
|---|
Much less effort has been devoted to the expression of genes that are down-regulated by water-deficit stress; however, it is known that a few genes have reduced mRNA levels. In Arabidopsis thaliana, proline accumulation occurs in response to water deficit. Genes involved in proline accumulation are induced by water-deficit stress and genes involved in proline breakdown are repressed (Kiyosue et al., 1996). This, and other possible controls, results in an accumulation of proline in Arabidopsis thaliana. In addition, two other genes, hydroxynitrile lyase and a remorin-like gene, were down-regulated and genes of similar predicted function were simultaneously up-regulated (see Reymond et al., 2000).
|
CONCLUSIONS |
|---|
|
TOPABSTRACTINTRODUCTIONGENES REGULATED BY WATER-DEFICIT...PREDICTED FUNCTIONS OF...FUNCTION OF DOWN-REGULATED GENESCONCLUSIONSLITERATURE CITED |
|---|
Future experiments using microarray and gene discovery techniques will continue to add to the broad picture of the cellular plant stress response. The use of full genome arrays will permit the characterization of the vast majority of the genes that are altered by water-deficit stress. Since the experiments that have been published thus far are based on a rapid, severe water-deficit treatment, it is important that microarray experiments be completed in experimental conditions that more closely approximate stress development in the field. The widespread use of these techniques will permit many different experimental designs to be used which will permit a better understanding of the complexities of water-deficit stress and the potential functions of the induced genes. It is important that multidisciplinary teams of scientists with broad expertise in plant stress biology join forces to analyse and interpret the microarray data. In this way, we will be able to distinguish genes that are induced by secondary stresses and genes that are induced by lesions in metabolic pathways in order to identify the genes involved in adaptation. The gene patterns will point to biochemical and cell biology experiments that should be undertaken to understand fully the cellular response. Further investigations using whole plant studies will finally be needed before this information can used to assess the impact of gene expression on the whole plant and to apply the findings to practical agriculture.
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONGENES REGULATED BY WATER-DEFICIT...PREDICTED FUNCTIONS OF...FUNCTION OF DOWN-REGULATED GENESCONCLUSIONSLITERATURE CITED |
|---|
-
Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.[CrossRef][Medline]
2. Asada K. 1999. The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annual Review Plant Physiology and Plant Molecular Biology 50: 601–639.[CrossRef][Web of Science]
Ascenzi R, Gantt JS. 1999. Molecular genetic analysis of the drought-inducible linker histone variant in Arabidopsis thaliana. Plant Molecular Biology 41: 159–169.[CrossRef][Web of Science][Medline]
Bartholomew DM, Bartley GE, Scolnik PA. 1991. Abscisic acid control of RBCS and CAB transcription in tomato leaves. Plant Physiology 96: 291–296.
Borsani O, Diaz P, Agius MF, Valpuesta C, Monza J. 2001. Water stress generates an oxidative stress through the induction of a specific Cu/Zn superoxide dismutase in Lotus corniculatus leaves. Plant Science 161: 757–763.[CrossRef]
Bozarth CS, Mullet JE, Boyer JS. 1987. Cell wall proteins at low water potentials. Plant Physiology 85: 261–267.
Bray EA, Bailey-Serres J, Weretilnyk E. 2000. Responses to abiotic stress. In: Buchanan BB, Gruissem W, Jones RL, eds. Biochemistry and molecular biology of plants. Rockville: American Society of Plant Physiologists, 1158–1203.
Chaves MM. 1991. Effects of water deficits on carbon assimilation. Journal of Experimental Botany 42: 1–16.
Cohen A, Moses MS, Plant AL, Bray EA. 1999. Multiple mechanisms control the expression of abscisic acid (ABA)-requiring genes in tomato plants exposed to soil water deficit. Plant, Cell and Environment 22: 989–998.[CrossRef]
Daniels MJ, Mirkov TE, Chrispeels MJ. 1994. The plasma membrane of Arabidopsis thaliana contains a mercury insenstive aquaporin that is a homolog of the tonoplast water channel protein TIP. Plant Physiology 106: 1325–1333.[Abstract]
Foyer CH, Valadier M-H, Migge A, Becker TW. 1998. Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. Plant Physiology 117: 283–292.
Garay-Arroyo A, Colmenero-Flores JM, Garciarrubio A, Covarrubias AA. 2000. Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. Journal of Biological Chemistry 275: 5668–5674.
García-Gómez BI, Campos F, Hernández M, Covarrubias AA. 2000. Two bean cell wall proteins more abundant during later deficit are high in proline and interact with a plasma membrane protein. Plant Journal 22: 277–288.[CrossRef][Web of Science][Medline]
Hanson AD, Hitz WD. 1982. Metabolic responses of mesophytes to plant water deficits. Annual Review of Plant Physiology 33: 163–203.[Web of Science]
Hirayama T, Ohto C, Mizoguchi T, Shinozaki K. 1995. A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the USA 92: 3903–3907.
Hsiao TC. 1973. Plant responses to water stress. Annual Review of Plant Physiology 24: 519–570.[Web of Science]
Hsiao TC, Xu L-K. 2000. Sensitivity of growth of roots versus leaves to water stress: biophysical analysis and relation to water transport. Journal of Experimental Botany 51: 1596–1616.
Jagtap V, Bhargava S. 1995. Variation in the antioxidant metabolism of drought tolerant and drought susceptible varieties of Sorghum bicolor (L.) Moench. exposed to high light, low water and high temperature stress. Journal of Plant Physiology 145: 195–197.
Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K. 1993a. Character ization of cDNA for a dehydration-inducible gene that encodes a Clp-A, B-like protein in Arabidopsis thaliana L. Biochemical and Biophysical Research Communications 196: 1214–1220.[CrossRef][Web of Science][Medline]
Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K. 1993b. Characterization of two cDNAs (Erd11 and Erd13) for dehydration-inducible genes that encode putative glutathione S-transferases in Arabidopsis thaliana L. FEBS Letters 335: 189–192.[CrossRef][Web of Science][Medline]
Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K. 1994a. Cloning of cDNAs for genes that are early-responsive to dehydration stress (ERDs) in Arabidopsis thaliana L.: identification of three ERDs as HSP cognate genes. Plant Molecular Biology 25: 791–798.[CrossRef][Web of Science][Medline]
Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K. 1994b. Erd15, a cDNA for a dehydration-induced gene from Arabidopsis thaliana. Plant Physiology 106: 1707–1707.[CrossRef][Web of Science][Medline]
Kiyosue T, Abe H, Yamaguchi-Shinozaki K, Shinozaki K. 1998. ERD6, a cDNA clone for an early dehydration-induced gene of Arabidopsis, encodes a putative sugar transporter. Biochimica et Biophysica Acta-Biomembranes 1370: 187–191.[CrossRef]
Kiyosue T, Yoshiba Y, Yamaguchi-Shinozaki K, Shinozaki K. 1996. A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8: 1323–1335.[Abstract]
Kiyosue T, Beethman JK, Pinot F, Hammock BD, Yamaguchi-Shinozaki K, Shinozaki K. 1994c. Characterization of an Arabidopsis cDNA for a soluble epoxies hydrolase gene that is induced by auxin and water stress. Plant Journal 6: 259–269.[CrossRef][Web of Science][Medline]
Koizumi M, Yamaguchi-Shinozaki K, Tsuji H, Shinozaki K. 1993. Structure and expression of 2 genes that encode distinct drought-inducible cysteine proteinases in Arabidopsis thaliana. Gene 129: 175–182.[CrossRef][Web of Science][Medline]
Lee Y-H, Oh H-S, Cheon C-I, Hwang I-T, Kim Y-J, Chun J-Y. 2001. Structure and expression of the Arabidopsis thaliana homeobox gene ATHB-12. Biochemical and Biophysical Research Communications 284: 133–141.[CrossRef][Web of Science][Medline]
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K. 1998. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidop sis. Plant Cell 10: 1391–1406.
Lockhart JA. 1965. Cell extension. In: Bonner J, Varner JE, eds. Plant biochemistry. New York: Academic Press, 826–849.
Marshall JG, Dumbroff EB. 1999. Turgor regulation via cell wall adjustment in White Spruce. Plant Physiology 119: 313–320.
Mikami K, Katagiri T, Iuchi S, Yamaguchi-Shinozaki K, Shinozaki K. 1998. A gene encoding phosphatidylinositol-4-phosphate 5-kinase is induced by water stress and abscisic acid in Arabidopsis thaliana. Plant Journal 15: 563–568.[CrossRef][Web of Science][Medline]
Mittler R, Zilinskas BA. 1994. Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during progression of drought stress and following recovery from drought. Plant Journal 5: 397–405.[CrossRef][Web of Science][Medline]
Mizoguchi T, Hayashida N, Yamaguchi-Shinozaki K, Kamada H, Shinozaki K. 1993. ATMPKs: a gene family of plant MAP kinases in Arabidopsis thaliana. FEBS Letters 336: 440–444.[CrossRef][Web of Science][Medline]
Mizoguchi T, Hayashida N, Yamaguchi-Shinozaki K, Kamada H, Shinozaki K. 1995. Two genes that encode ribosomal protein S6 kinase homologs are induced by cold or salinity stress in Arabidopsis thaliana. FEBS Letters 358: 199–204.[CrossRef][Web of Science][Medline]
Mizoguchi T, Irie K, Hirayama T, Hayashida N, Yamaguchi-Shinozaki K, Matsumoto K, Shinozaki K. 1996. A gene encoding a mitogen-activated protein kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the USA 93: 765–769.
Ostergaard L, Lauvergeat V, Naested H, Mattsson O, Mundy J. 2001. Two differentially regulated Arabidopsis genes define a new branch of the DFR superfamily. Plant Science 160: 463–472.
Reymond P, Weber H, Damond M, Farmer EE. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12: 707–720.
Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samara RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Chandahari D, Sherman BK, Yu CL. 2000. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290: 2105–2110.
Sairam RK, Saxena DC. 2000. Oxidative stress and antioxidants in wheat genotypes: possible mechanism of water stress tolerance. Journal of Agronomy and Crop Science 184: 55–61.[CrossRef][Web of Science]
Scippa GS, Griffiths A, Chiatante D, Bray EA. 2000. The H1 histone variant of tomato, H1-S, is targeted to the nucleus and accumulates in chromatin in response to water-deficit stress. Planta 211: 173–181.[CrossRef][Web of Science][Medline]
Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K. 2001. Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13: 61–72.
Smirnoff N. 1993. Tansley Review 52. The role of active oxygen in the response of plants to water deficit and desiccation. New Phytologist 125: 27–58.[CrossRef][Web of Science]
Söderman E, Hjellström M, Fahleson J, Engström P. 1999. The HD-Zip gene ATHB6 in Arabidopsis is expressed in developing leaves, roots and carpels and up-regulated by water deficit conditions. Plant Molecular Biology 40: 1073–1083.[CrossRef][Web of Science][Medline]
Söderman E, Mattsson J, Engström P. 1996. The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. Plant Journal 10: 375–81.[CrossRef][Web of Science][Medline]
Solomon M, Belenghi B, Delledonne M, Menachem E, Levine A. 1999. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11: 431–444.
Todd GW. 1972. Water deficits and enzymatic activity. In: Kozlowski TT, eds. Water deficits and plant growth. New York: Academic Press, 177–216.
Tyree MT, Jarvis PG. 1982. Water in tissues and cells. In: Lange OL, Nobel PS, Osmond CB, Ziegler H, eds. Physiological plant ecology II. New York: Springer-Verlag, 35–78.
Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K. 2000. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proceedings of the National Academy of Sciences of the USA 97: 11632–11637.
Urao T, Katagiri T, Mizoguchi T, Yamaguchi-Shinozaki K, Hayashida N, Shinozaki K. 1994a. An Arabidopsis thaliana cDNA encoding Ca2+-dependent protein kinase. Plant Physiology 105: 1461–1462. [CrossRef][Web of Science][Medline]
Urao T, Katagiri T, Mizoguchi T, Yamaguchi-Shinozaki K, Hayashida N, Shinozaki K. 1994b. Two genes that encode Ca2+-dependent protein kinases are induced by drought and high-salt stresses in Arabidopsis thaliana. Molecular and General Genetics 244: 331–340.
Urao T, Noji M, Yamaguchi-Shinozaki K, Shinozaki K. 1996. A transcriptional activation domain of ATMYB2, a drought-inducible Arabidopsis Myb-related protein. Plant Journal 10: 1145–1148. [CrossRef][Web of Science][Medline]
Vierstra RD. 1996. Proteolysis in plants: mechanisms and function. Plant Molecular Biology 32: 275–302[CrossRef][Web of Science][Medline]
Weaver LM, Froehlich JE, Amasino RM. 1999. Chloroplast-targeted ERD1 protein declines but its mRNA increases during senescence in Arabidopsis. Plant Physiology 119: 1209–1216.
Weig A, Deswarte C, Chrispeels MJ. 1997. The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiology 114: 1347–1357.[Abstract]
Williams J, Bulman M, Huttly A, Phillips A, Neill S. 1994. Characterization of a cDNA from Arabidopsis thaliana encoding a potential thiol protease whose expression is induced independently by wilting and abscisic acid. Plant Molecular Biology 25: 259–270.[CrossRef][Web of Science][Medline]
Wolkers WF, McCready S, Brandt WF, Lindsey GG, Hoekstra FA. 2001. Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro. Biochimica et Biophysica Acta (BBA) – Protein Structure and Molecular Enzymology 1544: 196–206.
Wu YJ, Cosgrove DJ. 2000. Adaptation of roots to low water potentials by changes in cell wall extensibility and cell wall proteins. Journal of Experimental Botany 51: 1543–1553.
Yamaguchi-Shinozaki K, Shinozaki K. 1994. A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6: 251–264.[Abstract]
Yamaguchi-Shinozaki K, Koizumi M, Urao S, Shinozaki K. 1992. Molecular cloning and characterization of 9 cDNAs for genes that are responsive to desiccation in Arabidopsis thaliana: Sequence analysis of one cDNA clone that encodes a putative transmembrane channel protein. Plant and Cell Physiology 33: 217–224.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  D.-J. Qing, H.-F. Lu, N. Li, H.-T. Dong, D.-F. Dong, and Y.-Z. Li Comparative Profiles of Gene Expression in Leaves and Roots of Maize Seedlings under Conditions of Salt Stress and the Removal of Salt Stress Plant Cell Physiol., April 1, 2009; 50(4): 889 - 903. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Alos, M. Roca, D. J. Iglesias, M. I. Minguez-Mosquera, C. M. B. Damasceno, T. W. Thannhauser, J. K. C. Rose, M. Talon, and M. Cercos An Evaluation of the Basis and Consequences of a Stay-Green Mutation in the navel negra Citrus Mutant Using Transcriptomic and Proteomic Profiling and Metabolite Analysis Plant Physiology, July 1, 2008; 147(3): 1300 - 1315. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Fresneau, J. Ghashghaie, and G. Cornic Drought effect on nitrate reductase and sucrose-phosphate synthase activities in wheat (Triticum durum L.): role of leaf internal CO2 J. Exp. Bot., August 30, 2007; (2007) erm150v1. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. E. Wong, Y. Li, A. Labbe, D. Guevara, P. Nuin, B. Whitty, C. Diaz, G. B. Golding, G. R. Gray, E. A. Weretilnyk, et al. Transcriptional Profiling Implicates Novel Interactions between Abiotic Stress and Hormonal Responses in Thellungiella, a Close Relative of Arabidopsis Plant Physiology, April 1, 2006; 140(4): 1437 - 1450. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Rodriguez-Uribe and M. A. O'Connell A root-specific bZIP transcription factor is responsive to water deficit stress in tepary bean (Phaseolus acutifolius) and common bean (P. vulgaris) J. Exp. Bot., March 1, 2006; 57(6): 1391 - 1398. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. J. Marquez, M. Betti, M. Garcia-Calderon, P. Pal'ove-Balang, P. Diaz, and J. Monza Nitrate assimilation in Lotus japonicus J. Exp. Bot., July 1, 2005; 56(417): 1741 - 1749. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. E. Williams, J. Torabinejad, E. Cohick, K. Parker, E. J. Drake, J. E. Thompson, M. Hortter, and D. B. DeWald Mutations in the Arabidopsis Phosphoinositide Phosphatase Gene SAC9 Lead to Overaccumulation of PtdIns(4,5)P2 and Constitutive Expression of the Stress-Response Pathway Plant Physiology, June 1, 2005; 138(2): 686 - 700. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Ruggiero, H. Koiwa, Y. Manabe, T. M. Quist, G. Inan, F. Saccardo, R. J. Joly, P. M. Hasegawa, R. A. Bressan, and A. Maggio Uncoupling the Effects of Abscisic Acid on Plant Growth and Water Relations. Analysis of sto1/nced3, an Abscisic Acid-Deficient but Salt Stress-Tolerant Mutant in Arabidopsis Plant Physiology, October 1, 2004; 136(2): 3134 - 3147. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. S. Scippa, M. Di Michele, E. Onelli, G. Patrignani, D. Chiatante, and E. A. Bray The histone-like protein H1-S and the response of tomato leaves to water deficit J. Exp. Bot., January 1, 2004; 55(394): 99 - 109. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. GRIFFITHS and M. A. J. PARRY Plant Responses to Water Stress Ann. Bot., June 15, 2002; 89(7): 801 - 802. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. W. LAWLOR Limitation to Photosynthesis in Water-stressed Leaves: Stomata vs. Metabolism and the Role of ATP Ann. Bot., June 15, 2002; 89(7): 871 - 885. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||