JXB Advance Access originally published online on September 24, 2004
Journal of Experimental Botany 2004 55(407):2343-2351; doi:10.1093/jxb/erh276
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RESEARCH PAPER |
Root growth maintenance during water deficits: physiology to functional genomics*
1Department of Agronomy, Plant Sciences Unit, 1-87 Agriculture Building, University of Missouri, Columbia, MO 65211, USA
2Department of Plant Biology and Department of Crop Sciences, University of Illinois, Urbana, IL 61801, USA
3Department of Computer Science, University of Missouri, Columbia, MO 65211, USA
To whom correspondence should be addressed. Fax: +1 573 882 1469. E-mail: SharpR{at}missouri.edu
Received 16 July 2004; Accepted 23 August 2004
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Abstract |
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Top
Abstract
IntroductionProgress in understanding the network of mechanisms involved in maize primary root growth maintenance under water deficits is reviewed. These include the adjustment of growth zone dimensions, turgor maintenance by osmotic adjustment, and enhanced cell wall loosening. The role of the hormone abscisic acid (ABA) in maintaining root growth under water deficits is also addressed. The research has taken advantage of kinematic analysis, i.e. characterization of spatial and temporal patterns of cell expansion within the root growth zone. This approach revealed different growth responses to water deficits and ABA deficiency in distinct regions of the root tip. In the apical 3 mm region, elongation is maintained at well-watered rates under severe water deficit, although only in ABA-sufficient roots, whereas the region from 3–7 mm from the apex exhibits maximum elongation in well-watered roots, but progressive inhibition of elongation in roots under water deficit. This knowledge has greatly facilitated discovery of the mechanisms involved in regulating the responses. The spatial resolution with which this system has been characterized and the physiological knowledge gained to date provide a unique and powerful underpinning for functional genomics studies. Characterization of water deficit-induced changes in transcript populations and cell wall protein profiles within the growth zone of the maize primary root is in progress. Initial results from EST and unigene analyses in the tips of well-watered and water-stressed roots highlight the strength of the kinematic approach to transcript profiling.
Key words: Abscisic acid, cell wall extensibility, ESTs, expansins, kinematics, osmotic adjustment
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Introduction |
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Drought is the major abiotic stress factor limiting crop productivity worldwide, and understanding the genetic and biochemical mechanisms which control drought tolerance is a central question in plant biology. As water resources for agricultural uses become more limiting, the development of drought-tolerant lines will become increasingly important. One aspect of principal importance in this arena is the response of root growth and development to water-deficit conditions.
The physiology of maize primary root elongation at low water potentials has been studied extensively by Sharp and co-workers, and the findings are summarized in this report. This work has provided the foundation for an understanding of the complex network of responses involved. The research has taken advantage of a kinematic approach, i.e. the study of spatial and temporal patterns of cell expansion within the growth zone (Erickson and Silk, 1980
; Silk, 1984), which has greatly facilitated discovery of the mechanisms involved in the growth responses. The spatial resolution with which this system has been characterized and the physiological knowledge gained to date provide a unique and powerful underpinning for functional genomics studies which are underway and will be introduced here. This combined approach can be expected to yield much novel and valuable information towards the goal of a comprehensive understanding of the regulation of root growth during water deficits.
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Root growth maintenance during water deficits |
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In plants growing in drying soil, the development of the root system is usually less inhibited than shoot growth, and may even be promoted (Sharp and Davies, 1989
). Maintenance of root growth during water deficits is an obvious benefit to maintain an adequate plant water supply, and is under genetic control (O'Toole and Bland, 1987; Sponchiado et al., 1989).
An important feature of the root system response to soil drying is the ability of some roots to continue elongation at water potentials that are low enough to inhibit shoot growth completely. For example, this occurs in nodal (adventitious) roots of maize, which must penetrate through dry surface soil (Sharp and Davies, 1979; Westgate and Boyer, 1985), and in primary roots of a range of species, which helps seedling establishment under dry conditions by ensuring a supply of water before shoot emergence (Sharp et al., 1988; Spollen et al., 1993; van der Weele et al., 2000). Figure 1 shows for several agronomic species that the primary root maintains substantial elongation rates at water potentials lower than –1.5 MPa, whereas shoot growth is completely inhibited at much higher water potentials.
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Taking advantage of a kinematic approach |
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As emphasized by Erickson and Silk (1980)
, knowledge of the spatial and temporal variation in growth rates within tissues can be a powerful tool in physiological studies. Under well-watered conditions, the elongation zone of the maize primary root encompasses the apical 12 mm (Fig. 2). Cells are produced in the meristem near the apex, and during expansion are displaced basally by the production and expansion of new cells. The relative elongation rate peaks at about 4.5 mm from the apex, and then gradually declines to zero. In water-stressed roots, it was discovered that elongation is maintained preferentially towards the apex (Sharp et al., 1988). Remarkably, even at a water potential of –1.6 MPa, the relative elongation rate is unaffected in the apical 3 mm, but is progressively inhibited at more basal locations, reaching zero at 7 mm from the apex. Clearly, different mechanisms can be expected to underlie the responses to water stress in the apical and basal regions, and investigation of mechanisms maintaining cell elongation must focus on the apical region. However, the inhibition in the basal region is also important to understand, because this is probably part of a co-ordinated response to allow the preferential use of limited resources (water and growth substrates) in the apical region.
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In addition, roots growing at low water potential become thinner (Sharp et al., 1988
), and this change in morphology is also believed to be adaptive such that roots can further concentrate their use of resources (Sharp et al., 1990). The thinning is caused by restriction of the lateral expansion rate of cells in both the stele and cortex, although only in the apical 5 mm. Basal to this, lateral expansion rates are nearly identical to those in well-watered roots (Liang et al., 1997). This pattern is opposite to the response of longitudinal expansion, showing that the response of cell expansion to water stress is regulated independently in longitudinal and radial directions. The regulatory mechanisms that determine these responses are unknown. |
Osmotic adjustment |
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Early work showed that there is substantial osmotic adjustment in the tips of both maize nodal roots (Sharp and Davies, 1979
; Westgate and Boyer, 1985) and primary roots (Sharp et al., 1990). Osmotic adjustment in growing regions can result from two overall mechanisms, either an increase in the net rate of osmoticum deposition (including effects on solute synthesis, uptake, catabolism, import, and utilization), or a decrease in the rate of tissue expansion and, therefore, in the rate of osmoticum dilution. Clearly, the former is more likely to represent an adaptive response that could contribute to growth maintenance. In the maize primary root tip, hexoses are the primary contributor to osmotic adjustment in the basal region of the growth zone, but the accumulation of hexose can be accounted for by the reduced rates of volume expansion in this region; in fact, hexose deposition rates beyond 3 mm from the apex are decreased in water-stressed compared with well-watered roots (Sharp et al., 1990). By contrast, in the apical few millimetres, proline concentration increases dramatically in water-stressed roots, and contributes up to 50% of the osmotic adjustment. This response involves a several-fold increase in the net rate of proline deposition (Voetberg and Sharp, 1991), which in turn involves an increase in the rate of proline transport to the root tip (Verslues and Sharp, 1999). Additional work showed that accumulation of the hormone abscisic acid (ABA) is required for the increase in proline deposition at low water potential (Ober and Sharp, 1994), suggesting that ABA may play a role in regulating proline transport to the root tip. In this regard, it is noteworthy that there are reports that water stress can increase expression of proline transporters (Rentsch et al., 1996) as well as cause large increases in proline concentration in the phloem sap (Girousse et al., 1996). The solutes that account for most of the other 50% of the osmotic adjustment in the apical few millimetres of the water-stressed roots remain to be identified. The other measured solutes (hexose, sucrose, other amino acids, potassium) made only a small contribution to osmotic adjustment in this region (Voetberg and Sharp, 1991). |
Enhanced cell wall loosening |
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The extent of osmotic adjustment in the maize primary root tip, although substantial, is insufficient to maintain turgor at well-watered levels in roots growing under severe water deficits. At a water potential of –1.6 MPa, turgor is reduced by over 50% throughout the growth zone (Spollen and Sharp, 1991
). In the apical few millimetres, the complete maintenance of elongation rate (Fig. 2) despite the decrease in turgor suggested that longitudinal cell wall extensibility is enhanced in this region under water stress. This was confirmed by direct assessment of cell wall extension properties, which showed a large increase in acid-induced extensibility in the apical 5 mm (and a decrease in the 5–10 mm region) of water-stressed compared with well-watered roots (Wu et al., 1996).
Cell wall-loosening proteins are believed to play key roles in controlling cell wall extension. Therefore, the activities of expansins and xyloglucan endotransglycosylase (XET) were examined to see if they correlated with the increase in wall extensibility in the apical region of the water-stressed roots. Expansin activity and extractable expansin protein increased substantially in the apical 5 mm of water-stressed compared with well-watered roots (Wu et al., 1996). The susceptibility to expansin action also increased, indicating changes in wall structure or chemistry that facilitated expansin accessibility or action. A subsequent study (Wu et al., 2001) showed that four expansin genes are expressed specifically in the growth zone in well-watered roots, and that three of these are rapidly up-regulated in the apical 5 mm and down-regulated in the 5–10 mm region after transplanting to low water potential (Fig. 3), correlating with the maintenance of elongation and the increase in cell wall extensibility in the apical region. These results illustrate the advantage of using a kinematic approach, because the up- and down-regulation of expression of the same genes in adjacent regions would have precluded observation of these changes if the whole tip had been studied. XET activity was also enhanced specifically in the apical 5 mm of the water-stressed roots, and this response was shown to be dependent on ABA accumulation (Wu et al., 1994). By contrast, the evidence suggested that the changes in expansin gene expression are not mediated by ABA. Proteomic analyses are in progress to gain a comprehensive understanding of how cell wall protein composition changes in association with the differential growth responses to water deficits in the different regions of the root tip.
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Growth-maintaining role of ABA accumulation in water-stressed roots |
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Hormones are likely to play important regulatory roles in the adaptation of root growth to water deficits, but the involvement of most of these compounds has not been elucidated. The exception is the accumulation of ABA, which has been shown to be required for the maintenance of maize primary root elongation at low water potentials (reviewed in Sharp, 2002
). When maize seedlings are grown at a water potential of –1.6 MPa, the ABA content of the root growth zone increases about 5-fold. Three approaches have been used to study the effect on root growth of reducing the accumulation of ABA: (i) the inhibitor fluridone, which blocks carotenoid synthesis and, thereby, inhibits ABA synthesis although at an early step of the pathway; (ii) the vp5 mutant, which has a defect at the same step as that blocked by fluridone; (iii) the vp14 mutant, which has a defect in the synthesis of xanthoxin (Tan et al., 1997). Xanthoxin synthesis is considered a key regulatory step in water stress-induced ABA production (Qin and Zeevaart, 1999). The initial studies used fluridone and vp5 (Saab et al., 1990, 1992; Sharp et al., 1994), and studies of vp14 were recently undertaken to strengthen the conclusion that the results were due to ABA deficiency and not to other effects. The results obtained with the three approaches were very similar (Fig. 4). At high water potential, root elongation rates (and ABA contents) were minimally affected. At low water potential, by contrast, reduced ABA accumulation was associated with more severe inhibition of root elongation than in wild-type or untreated seedlings. In all cases, root elongation rate fully recovered when the ABA content of the growth zone was restored to normal levels with exogenous ABA, confirming that the normal accumulation of ABA is necessary for root growth maintenance during water stress.
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It is important to note that the conclusion that the accumulation of ABA in water-stressed roots helps to maintain elongation cannot be inferred by applying ABA to well-watered seedlings in order to simulate the increase in content under water stress (Sharp et al., 1994
). Figure 4 shows that, in well-watered seedlings treated with ABA, root growth was substantially inhibited at the root tip ABA content that occurs in water-stressed roots. These results illustrate that the maintenance of root elongation at low water potential by ABA is not solely a function of the increase in ABA content, but also requires the change in environmental conditions that modifies the growth response to ABA.
The role of ABA in determining plant growth responses to water deficits is a long-standing question, and the finding that the accumulation of ABA is necessary for root growth maintenance at low water potentials contrasts with the commonly proposed growth-inhibitory function of increased ABA concentrations in water-stressed plants (Trewavas and Jones, 1991). Recent studies have also shown that the normal ABA levels in well-watered plants are required to maintain shoot growth in tomato (Sharp et al., 2000) and Arabidopsis (LeNoble et al., 2004). In all cases, the action of ABA has been shown to involve the suppression of ethylene production (Sharp et al., 2000; Spollen et al., 2000, LeNoble et al., 2004), but taken together, the studies indicate that water-deficient compared with well-watered plants require increased levels of ABA to prevent excess ethylene production (Sharp, 2002). This difference may be related to a role of ABA accumulation in promoting the antioxidant system to maintain reactive oxygen species (ROS) at non-damaging levels during water deficits (Fig. 5). This hypothesis is based on evidence that ROS are produced in greater amounts in stressed tissues, that ABA treatments have been shown to increase expression of genes for antioxidant enzymes, for example, catalase in maize leaves (Guan et al., 2000), and that excess ROS levels can cause increased ethylene synthesis (Overmyer et al., 2000).
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In recent studies, the effect of ABA deficiency on levels of ROS in the maize primary root growth zone was studied using the vp14 mutant, in which ABA levels are deficient in water-stressed but not well-watered roots (I-J Cho, M Sivaguru, RE Sharp, unpublished data). Under well-watered conditions, ROS levels were low in roots of both wild-type and vp14 seedlings. Under water deficits, ROS levels were slightly greater in the growth zone of wild-type roots and increased dramatically in vp14. The increased ROS levels in vp14 were prevented when ABA was restored to the wild-type level by exogenous application. The effect of ABA deficiency on ROS levels occurred specifically in the region 1–3 mm from the root apex where cell elongation is normally maintained under water deficits but is inhibited by ABA deficiency (Saab et al., 1992
; Sharp et al., 1994; Ober and Sharp, 2003). Loss of plasma membrane integrity occurred in the same region of the ABA-deficient roots, and results indicate that the increase in ROS levels preceded and caused the membrane impairment. The relationship of these events to the increase in ethylene production and inhibition of root elongation caused by ABA-deficiency under water deficits is under investigation. |
From physiology to functional genomics |
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As detailed above, the maize primary root system is ideally suited for the application of genomic analyses to gain a comprehensive understanding of the mechanisms that control the responses of root growth to water stress. Characterization of water deficit-induced changes in transcript populations within the growth zone of the maize primary root is in progress. Initial results from expressed sequence tag (EST) and unigene analyses in the tips of well-watered and water-stressed roots highlight the strength of the kinematic approach to transcript profiling.
At 5 h and 48 h after transplanting to well-watered or water deficit (water potential of –1.6 MPa) conditions, primary roots were harvested and cut into four regions from the apex (Fig. 6): region 1 (0–3 mm), in which elongation rates are completely maintained under water deficit; region 2 (3–7 mm), in which elongation rates are maximal in well-watered roots but progressively inhibited under water deficit; region 3 (7–12 mm), in which elongation decelerates in well-watered roots and is completely inhibited under water deficit; and region 4 (12–20 mm), which is non-elongating in well-watered and water-stressed roots.
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By comparison with regions 1–3, region 4 helps to identify stress-induced changes that are specifically associated with growth, and its maintenance or inhibition (as in the similar studies of expansin expression shown in Fig. 3). The 48 h time point was chosen to characterize changes that are associated with the steady-state patterns of relative elongation rate in acclimated seedlings (Figs 2, 6). The 5 h time point was chosen to facilitate identification of regulatory/primary changes in gene expression (as opposed to secondary effects) after the initiation of the water-stress treatment. The well-watered samples from 5 h and 48 h were combined, and 12 primary cDNA libraries (well-watered; water-stressed 5 h; water-stressed 48 h; four regions each) were generated such that each library carried a region-identifying sequence tag. After combining the libraries for each condition, three normalized libraries were generated and
6000 ESTs from each were sequenced. The whole 3'-EST collection was then grouped into clusters of sequences with high similarity. The relative size of each cluster in a library-region combination was calculated and the distribution of cluster sizes for each of the 12 combinations then compared to produce similarity scores. These scores are represented in the hierarchical tree shown in Fig. 6. The results illustrate that EST populations were distinctly different both in adjacent regions within a treatment and in particular regions between treatments. The most distinct profile was found in region 2 of the well-watered roots, corresponding to the uniqueness of this region in exhibiting maximal elongation rates under well-watered conditions. Under water-deficit conditions, region 2 acquired a transcript profile which was more similar to that of the decelerating region (region 3) of well-watered roots. By contrast, the overall sequence collections from region 1 clustered together for the well-watered and water-stressed treatments (both 5 h and 48 h), which underscores that the transcriptional programme in this region was less disturbed by water stress than in other regions. This finding corresponds to the maintenance of relative elongation rate in region 1 of the water-stressed roots, although it is important to note that the overall similarity in EST populations does not entail that gene expression in this region was identical between the treatments. Indeed, it is anticipated that in region 1 microarray profiling and quantitative PCR studies will reveal significant changes in expression which are associated with mechanisms of root growth maintenance under water deficits.
Functional annotations of the EST populations indicate that processes which reflect the active root apical meristem, including translation, post-translational modification, RNA processing and modification, chromatin structure and dynamics, and cell cycle control were not greatly affected by the water-deficit treatment. However, water deprivation for 48 h led to the repression of transcripts in categories of intracellular trafficking and carbohydrate metabolism and to significant up-regulation of transcripts related to lipid metabolism. Transcripts associated with the cytoskeleton and cell wall formation declined during water stress in regions 2–4, although region 2 exhibited recovery in the expression of these transcripts at 48 h, indicating acclimation. Similarly, transcripts involved in ethylene response were more abundant after 5 h of water stress, but at 48 h the abundance was the same as that found in the well-watered roots. A number of ABA-responsive transcripts were found at a somewhat higher frequency in both 5 h and 48 h-stressed roots. It should be noted that these statements must be viewed with caution, because the nature of efficiently normalized cDNA libraries distorts transcript abundance.
To date, a total of 7688 unigenes have been identified in the root tips from the well-watered and water-stressed roots, including 992 from a subtracted cDNA library in which transcripts present under well-watered conditions were removed. Of the total of 6696 unigenes identified in the three tagged libraries, a surprisingly high number, 4517, were specific to individual libraries, and moreover, the majority of those were also specific to individual regions within the individual libraries (Table 1). These results again illustrate the advantage of the kinematic approach to this study. While experiments in the 1980s estimated the number of genes expressed in roots to be fewer than 10 000 (Kamalay and Goldberg, 1980, 1984), recent analyses have altered these estimates. The analysis of SAGE tags and an analysis of microarray data in Arabidopsis indicated a much higher number of genes expressed in (total) root tissues; at least 15 000 expressed sequence tags or transcripts have been identified (Birnbaum et al., 2003; Ekman et al., 2003). Accordingly, results of the present study suggest that from the sampling of 21 000 sequenced ESTs from which the root tip unigene set was derived, approximately half of the maize root transcriptome has been obtained.
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Probing the maize root transcriptome by SAGE
An additional dimension has been introduced by the generation of a SAGE library from well-watered roots (regions 1–4). SAGE (Serial Analysis of Gene Expression) technology results in concatenated clones that may contain 3'-end located portions of up to 70 genes per clone (Velculescu et al., 1995
). From the number of repeat detections of particular SAGE-tags, a true abundance profile of a tissue is an additional outcome with this technique. In the well-watered maize root, more than 14 000 individual SAGE tags were found (V Poroyko, HJ Bohnert, unpublished data). This number of unique tags represents a minimum number of expressed genes, but most likely does not represent the entire maize root transcriptome. To identify genes corresponding with the different SAGE tags, the maize root EST database was queried to obtain a virtual maize root transcript population. In total, >18 000 maize cDNA sequences that had been determined in the EST sequencing project were analysed, resulting in the identification of 5630 cDNAs that could be assigned to SAGE tags. Correlating SAGE tag and EST number in each library provided an interesting aspect (Fig. 7). Although the SAGE tags were derived from well-watered root RNA, they were almost evenly distributed between the libraries, indicating that transcript complexity is largely unchanged by water stress and that most genes are expressed irrespective of the physiological state of the root. What is different, however, is transcript abundance. This observation suggests that gene expression, affected by water stress, primarily alters abundance levels (reported as the number of a SAGE tag) and does not completely alter the structure of the expressed part of the genome. Closer inspection (Fig. 7) indicates that complexity changes after longer-term water stress (48 h), with extrapolation indicating that approximately 20% of the transcriptome could be specific for the water-stressed state.
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Conclusion |
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The studies reviewed here illustrate the complexity of mechanisms involved in root growth maintenance during water deficits. Understanding is being enhanced by an integrated approach, working across disciplines from physiology to functional genomics to gain a comprehensive knowledge of the gene networks, proteins, and metabolites involved. This knowledge will lead to novel approaches for improving drought tolerance through genetic and metabolic engineering of root function.
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Acknowledgements |
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This work was supported by National Science Foundation Plant Genome Program grant no. DBI-0211842, by the University of Missouri Food for the 21st Century Program, and by University of Illinois at Urbana-Champaign institutional grants. We thank In-Jeong Cho for supplying Fig. 5, and Dr Mary LeNoble for useful discussions and helpful comments on the manuscript.
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Footnotes |
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* This paper was also presented at the 4th International Crop Science Congress, Brisbane, Australia, September 2004.
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References |
|---|
Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, Benfey PN. 2003. A gene expression map of the Arabidopsis root. Science 302, 1956–1960.
Ekman DR, Lorenz WW, Przybyla AE, Wolfe NL, Dean JFD. 2003. SAGE analysis of transcriptome responses in Arabidopsis roots exposed to 2,4,6-trinitrotoluene. Plant Physiology 133, 1397–1406.
Erickson RO, Silk WK. 1980. The kinematics of plant growth. Scientific American 242, 134–151.
Girousse C, Bournoville R, Bonnemain J-L. 1996. Water deficit-induced changes in concentrations in proline and some other amino acids in the phloem sap of alfalfa. Plant Physiology 75, 951–955.
Guan LM, Zhao J, Scandalios JG. 2000. Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. The Plant Journal 22, 87–95.[CrossRef][Web of Science][Medline]
Kamalay JC, Goldberg RB. 1980. Regulation of structural gene expression in tobacco. Cell 19, 935–946.[CrossRef][Web of Science][Medline]
Kamalay JC, Goldberg RB. 1984. Organ-specific nuclear RNAs in tobacco. Proceedings of the National Academy of Sciences, USA 81, 2801–2805.
LeNoble ME, Spollen WG, Sharp RE. 2004. Maintenance of shoot growth by ABA: genetic assessment of the role of ethylene suppression. Journal of Experimental Botany 55, 237–245.
Liang BM, Sharp RE, Baskin TI. 1997. Regulation of growth anisotropy in well-watered and water-stressed maize roots. I. Spatial distribution of longitudinal, radial and tangential expansion rates. Plant Physiology 115, 101–111.[Abstract]
Ober ES, Sharp RE. 1994. Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. I. Requirement for increased levels of ABA. Plant Physiology 105, 981–987.[Abstract]
Ober ES, Sharp RE. 2003. Electrophysiological responses of maize roots to low water potentials: relationship to growth and ABA accumulation. Journal of Experimental Botany 54, 813–824.
O'Toole JC, Bland WL. 1987. Genotypic variation in crop plant root systems. Advances in Agronomy 41, 91–145.
Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann Jr H, Kangasjarvi J. 2000. Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. The Plant Cell 12, 1849–1862.
Qin X, Zeevaart JAD. 1999. The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proceedings of the National Academy of Sciences, USA 96, 15354–15361.
Rentsch D, Hirner B, Schmelzer E, Frommer WB. 1996. Salt stress-induced proline transporters and salt-stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. The Plant Cell 8, 1437–1446.[Abstract]
Saab IM, Sharp RE, Pritchard J. 1992. Effect of inhibition of abscisic acid accumulation on the spatial distribution of elongation in the primary root and mesocotyl of maize at low water potentials. Plant Physiology 99, 26–33.
Saab IN, Sharp RE, Pritchard J, Voetberg GS. 1990. Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant Physiology 93, 1329–1336.
Sharp RE. 2002. Interaction with ethylene: changing views on the role of ABA in root and shoot growth responses to water stress. Plant, Cell and Environment 25, 211–222.[CrossRef][Medline]
Sharp RE, Davies WJ. 1979. Solute regulation and growth by roots and shoots of water-stressed maize plants. Planta 147, 43–49.[CrossRef]
Sharp RE, Davies WJ. 1989. Regulation of growth and development of plants growing with a restricted supply of water. In: Jones HG, Flowers TL, Jones MB, eds. Plants under stress. Cambridge: Cambridge University Press, 71–93.
Sharp RE, Hsiao TC, Silk WK. 1990. Growth of the maize primary root at low water potentials. II. The role of growth and deposition of hexose and potassium in osmotic adjustment. Plant Physiology 93, 1337–1346.
Sharp RE, LeNoble ME, Else MA, Thorne ET, Gherardi F. 2000. Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: evidence for an interaction with ethylene. Journal of Experimental Botany 51, 1575–1584.
Sharp RE, Silk WK, Hsiao TC. 1988. Growth of the maize primary root at low water potentials. I. Spatial distribution of expansive growth. Plant Physiology 87, 50–57.
Sharp RE, Wu Y, Voetberg GS, Saab IN, LeNoble ME. 1994. Confirmation that abscisic acid accumulation is required for maize primary root elongation at low water potentials. Journal of Experimental Botany 45, 1743–1751.
Silk WK. 1984. Quantitative descriptions of development. Annual Review of Plant Physiology 35, 479–518.[CrossRef][Web of Science]
Silk WK, Lord EM, Eckard KJ. 1989. Growth patterns inferred from anatomical records. Plant Physiology 90, 708–713.
Spollen WG, LeNoble ME, Samuels TD, Bernstein N, Sharp RE. 2000. Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production. Plant Physiology 122, 967–976.
Spollen WG, Sharp RE. 1991. Spatial distribution of turgor and root growth at low water potentials. Plant Physiology 96, 438–443.
Spollen WG, Sharp RE, Saab IN, Wu Y. 1993. Regulation of cell expansion in roots and shoots at low water potentials. In: Smith JAC, Griffiths H, eds. Water deficits. Plant responses from cell to community. Oxford: Bios Scientific Publishers, 37–52.
Sponchiado BN, White JW, Castillo JA, Jones PG. 1989. Root growth of four common bean cultivars in relation to drought tolerance in environments with contrasting soil types. Experimental Agriculture 25, 249–257.
Tan BC, Schwartz SH, Zeevaart JAD, McCarty DR. 1997. Genetic control of abscisic acid biosynthesis in maize. Proceedings of the National Academy of Sciences, USA 94, 12235–12240.
Trewavas AJ, Jones HG. 1991. An assessment of the role of ABA in plant development. In: Davies WJ, Jones HG, eds. Abscisic acid: physiology and biochemistry. Oxford: Bios Scientific Publishers, 169–188.
van der Weele CM, Spollen WG, Sharp RE, Baskin TI. 2000. Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. Journal of Experimental Botany 51, 1555–1562.
Velculescu VE, Zhang L, Vogelstein B, Kinzler KW. 1995. Serial analysis of gene expression. Science 270, 484–487.
Verslues PE, Sharp RE. 1999. Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. II. Metabolic source of increased proline deposition in the elongation zone. Plant Physiology 119, 1349–1360.
Voetberg GS, Sharp RE. 1991. Growth of the maize primary root at low water potentials. III. Role of increased proline deposition in osmotic adjustment. Plant Physiology 96, 1125–1130.
Westgate ME, Boyer JS. 1985. Osmotic adjustment and the inhibition of leaf, root, stem, and silk growth at low water potentials in maize. Planta 164, 540–549.[CrossRef]
Wu Y, Sharp RE, Durachko DM, Cosgrove DJ. 1996. Growth maintenance of the maize primary root at low water potentials involves increases in cell wall extension properties, expansin activity and wall susceptibility to expansins. Plant Physiology 111, 765–772.[Abstract]
Wu Y, Spollen WG, Sharp RE, Hetherington PR, Fry SC. 1994. Root growth maintenance at low water potentials: increased activity of xyloglucan endotransglycosylase and its possible regulation by abscisic acid. Plant Physiology 106, 607–615.[Abstract]
Wu Y, Thorne ET, Sharp RE, Cosgrove DJ. 2001. Modification of expansin transcript levels in the maize primary root at low water potentials. Plant Physiology 126, 1471–1479.
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 J.I.L Morison, N.R Baker, P.M Mullineaux, and W.J Davies Improving water use in crop production Phil Trans R Soc B, February 12, 2008; 363(1491): 639 - 658. [Abstract] [Full Text] [PDF]
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 K. Yoshimura, A. Masuda, M. Kuwano, A. Yokota, and K. Akashi Programmed Proteome Response for Drought Avoidance/Tolerance in the Root of a C3 Xerophyte (Wild Watermelon) Under Water Deficits Plant Cell Physiol., February 1, 2008; 49(2): 226 - 241. [Abstract] [Full Text] [PDF]
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 R. Tuberosa, S. Salvi, S. Giuliani, M. C. Sanguineti, M. Bellotti, S. Conti, and P. Landi Genome-wide Approaches to Investigate and Improve Maize Response to Drought Crop Sci., December 18, 2007; 47(Supplement_3): S-120 - S-141. [Abstract] [Full Text] [PDF]
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J. Zhu, S. Alvarez, E. L. Marsh, M. E. LeNoble, I.-J. Cho, M. Sivaguru, S. Chen, H. T. Nguyen, Y. Wu, D. P. Schachtman, et al. Cell Wall Proteome in the Maize Primary Root Elongation Zone. II. Region-Specific Changes in Water Soluble and Lightly Ionically Bound Proteins under Water Deficit Plant Physiology, December 1, 2007; 145(4): 1533 - 1548. [Abstract] [Full Text] [PDF]
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 D. E. Nelson, P. P. Repetti, T. R. Adams, R. A. Creelman, J. Wu, D. C. Warner, D. C. Anstrom, R. J. Bensen, P. P. Castiglioni, M. G. Donnarummo, et al. Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres PNAS, October 16, 2007; 104(42): 16450 - 16455. [Abstract] [Full Text] [PDF]
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P. Basu, A. Pal, J. P. Lynch, and K. M. Brown A Novel Image-Analysis Technique for Kinematic Study of Growth and Curvature Plant Physiology, October 1, 2007; 145(2): 305 - 316. [Abstract] [Full Text] [PDF]
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J. Yang, J. Zhang, K. Liu, Z. Wang, and L. Liu Involvement of polyamines in the drought resistance of rice J. Exp. Bot., April 1, 2007; 58(6): 1545 - 1555. [Abstract] [Full Text] [PDF]
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B. Rymen, F. Fiorani, F. Kartal, K. Vandepoele, D. Inze, and G. T.S. Beemster Cold Nights Impair Leaf Growth and Cell Cycle Progression in Maize through Transcriptional Changes of Cell Cycle Genes Plant Physiology, March 1, 2007; 143(3): 1429 - 1438. [Abstract] [Full Text] [PDF]
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M.-B. Bogeat-Triboulot, M. Brosche, J. Renaut, L. Jouve, D. Le Thiec, P. Fayyaz, B. Vinocur, E. Witters, K. Laukens, T. Teichmann, et al. Gradual Soil Water Depletion Results in Reversible Changes of Gene Expression, Protein Profiles, Ecophysiology, and Growth Performance in Populus euphratica, a Poplar Growing in Arid Regions Plant Physiology, February 1, 2007; 143(2): 876 - 892. [Abstract] [Full Text] [PDF]
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V Poroyko, W. Spollen, L. Hejlek, A. Hernandez, M. LeNoble, G Davis, H. Nguyen, G. Springer, R. Sharp, and H. Bohnert Comparing regional transcript profiles from maize primary roots under well-watered and low water potential conditions J. Exp. Bot., January 1, 2007; 58(2): 279 - 289. [Abstract] [Full Text] [PDF]
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P Landi, M. Sanguineti, C Liu, Y Li, T. Wang, S Giuliani, M Bellotti, S Salvi, and R Tuberosa Root-ABA1 QTL affects root lodging, grain yield, and other agronomic traits in maize grown under well-watered and water-stressed conditions J. Exp. Bot., January 1, 2007; 58(2): 319 - 326. [Abstract] [Full Text] [PDF]
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L. Xiong, R.-G. Wang, G. Mao, and J. M. Koczan Identification of Drought Tolerance Determinants by Genetic Analysis of Root Response to Drought Stress and Abscisic Acid Plant Physiology, November 1, 2006; 142(3): 1065 - 1074. [Abstract] [Full Text] [PDF]
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A. Rosado, I. Amaya, V. Valpuesta, J. Cuartero, M. A. Botella, and O. Borsani ABA- and ethylene-mediated responses in osmotically stressed tomato are regulated by the TSS2 and TOS1 loci J. Exp. Bot., September 1, 2006; 57(12): 3327 - 3335. [Abstract] [Full Text] [PDF]
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S. Ma, Q. Gong, and H. J. Bohnert Dissecting salt stress pathways J. Exp. Bot., March 1, 2006; 57(5): 1097 - 1107. [Abstract] [Full Text] [PDF]
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L. Fan, R. Linker, S. Gepstein, E. Tanimoto, R. Yamamoto, and P. M. Neumann Progressive Inhibition by Water Deficit of Cell Wall Extensibility and Growth along the Elongation Zone of Maize Roots Is Related to Increased Lignin Metabolism and Progressive Stelar Accumulation of Wall Phenolics Plant Physiology, February 1, 2006; 140(2): 603 - 612. [Abstract] [Full Text] [PDF]
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J. Zhu, S. Chen, S. Alvarez, V. S. Asirvatham, D. P. Schachtman, Y. Wu, and R. E. Sharp Cell Wall Proteome in the Maize Primary Root Elongation Zone. I. Extraction and Identification of Water-Soluble and Lightly Ionically Bound Proteins Plant Physiology, January 1, 2006; 140(1): 311 - 325. [Abstract] [Full Text] [PDF]
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S. Park, J. Li, J. K. Pittman, G. A. Berkowitz, H. Yang, S. Undurraga, J. Morris, K. D. Hirschi, and R. A. Gaxiola Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants PNAS, December 27, 2005; 102(52): 18830 - 18835. [Abstract] [Full Text] [PDF]
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S. Giuliani, M. C. Sanguineti, R. Tuberosa, M. Bellotti, S. Salvi, and P. Landi Root-ABA1, a major constitutive QTL, affects maize root architecture and leaf ABA concentration at different water regimes J. Exp. Bot., December 1, 2005; 56(422): 3061 - 3070. [Abstract] [Full Text] [PDF]
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C. Zhu, D. Schraut, W. Hartung, and A. R. Schaffner Differential responses of maize MIP genes to salt stress and ABA J. Exp. Bot., November 1, 2005; 56(421): 2971 - 2981. [Abstract] [Full Text] [PDF]
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V. Poroyko, L.G. Hejlek, W.G. Spollen, G.K. Springer, H.T. Nguyen, R.E. Sharp, and H.J. Bohnert The Maize Root Transcriptome by Serial Analysis of Gene Expression Plant Physiology, July 1, 2005; 138(3): 1700 - 1710. [Abstract] [Full Text] [PDF]
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