Maintaining Root Growth in Drying Soil a Review of Progress and Gaps in Understanding
Plant Betoken Behav. 2013 Mar i; 8(three): e23454.
Genetic variability of oxalate oxidase action and elongation in water-stressed primary roots of diverse maize and rice lines
Priyamvada Voothuluru
1Division of Plant Sciences and Interdisciplinary Plant Group; University of Missouri; Columbia, MO U.s.a.
Hallie J. Thompson
1Division of Plant Sciences and Interdisciplinary Constitute Group; University of Missouri; Columbia, MO USA
Sherry A. Flint-Garcia
oneSectionalization of Institute Sciences and Interdisciplinary Plant Group; Academy of Missouri; Columbia, MO USA
2US Section of Agriculture; Agricultural Inquiry Service; Columbia, MO Us
Robert E. Sharp
1Partitioning of Plant Sciences and Interdisciplinary Plant Grouping; University of Missouri; Columbia, MO Usa
Received 2012 Nov 26; Revised 2012 December 27; Accustomed 2012 Dec 31.
- Supplementary Materials
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Additional material.
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Abstract
A previous study of maize primary roots under water stress showed pronounced increases in oxalate oxidase activity and apoplastic hydrogen peroxide in the upmost region of the growth zone where cell elongation is maintained. We examined whether increased oxalate oxidase action in water-stressed roots is conserved beyond diverse lines of maize and rice. The maize lines exhibited varied patterns of activeness, with some lines defective activity in the apical region. Moreover, none of the rice lines showed action in the apical region. Likewise, although the genotypic response of root elongation to water stress was variable in both maize and rice, this was not correlated with the pattern of oxalate oxidase activity. Implications of these findings for root growth regulation under water stress are discussed.
Keywords: maize, oxalate oxidase, rice, root elongation, water stress
Under water-express conditions, root growth is oft maintained relative to shoot growth.1 - 3 This response is an adaptive feature that allows plants to go along to access water as the soil dries.4 , 5 The mechanisms underlying growth maintenance under water stress have been studied extensively in the principal root of maize seedlings (for review see refs. 6−8). The length of the root growth zone is approximately 12 mm under well-watered conditions, whereas under water stress, jail cell elongation is maintained in the apical few mm merely is inhibited progressively farther from the noon, resulting in a shortened growth zone.9 These responses to h2o stress involve spatially differential regulation of cellular growth processes, including enhancement and inhibition of jail cell wall extensibility in the upmost and basal regions, respectively.ten Transcriptomic and cell wall proteomic analyses conducted with the different regions of the growth zone revealed primarily region-specific changes in h2o-stressed compared with well-watered roots.11 , 12 In particular, several transcripts and proteins related to reactive oxygen species (ROS) production, including putative oxalate oxidases, increased in abundance in the apical region and oxalate oxidase activeness was shown to increase markedly in the apical few mm.13 Oxalate oxidase activity also increased, although to a lesser extent, beyond approximately 8 mm from the apex (beyond the growth zone). Oxalate oxidases catalyze the conversion of oxalate to CO2 and hydrogen peroxide (H2O2), and in cereals are known to exist cell wall localized.14 Recent results of Voothuluru and Abrupt13 demonstrated that apoplastic H2Otwo levels increased specifically in the apical region of the growth zone in water-stressed maize main roots, correlating with the maintenance of cell elongation and the pronounced increment in oxalate oxidase activity in this region. Apoplastic ROS tin have growth regulatory functions including cell wall loosening also as tightening,15 , sixteen and have too been shown to act as signaling molecules in various processes.17 Accordingly, the increment in apoplastic ROS in the apical region of the growth zone is likely to play an important function in root growth regulation nether water stress.
The spatial profiles of transcripts, jail cell wall proteins, oxalate oxidase activity and apoplastic H2Oii in the growth zone of water-stressed maize chief roots, as described in a higher place, were conducted in inbred line FR697, which is a temperate line and was selected because it exhibits a relatively loftier capacity to maintain principal root elongation at depression h2o potentials.18 Since maize is genetically diverse,19 we wanted to determine if the increase in oxalate oxidase activity in the apical region of the growth zone of water-stressed primary roots was conserved beyond diverse lines. 20 six inbred lines, constituting the parents of the maize nested association mapping (NAM) population and representing the diversity of maize,20 were selected for assay. The NAM parents include 10 temperate lines, iii lines of mixed temperate and tropical ancestry, and thirteen tropical lines (Fig. ane).
Figure 1. Oxalate oxidase activity determined by oxalate-dependent oxidation of 4-chloro-1-naphthol, seen every bit nighttime bluish staining, in 12-mm upmost segments of h2o-stressed primary roots of the maize NAM parental lines. Roots were harvested 48 h after transplanting to vermiculite at a water potential of -1.6 MPa. Growth atmospheric condition, h2o potential measurements and oxalate oxidase staining procedures were as described by Voothuluru and Sharp.13 The illustrated roots are representative of 8–15 assayed roots per line. Experiments were repeated with a subset of 10 lines to ostend consistency of staining patterns.
After germination, the seedlings were transplanted into vermiculite at h2o potentials of -0.03 MPa (well-watered treatment) or -1.6 MPa (severe water stress treatment) and grown under conditions of minimal evaporation or transpiration (darkness and near-saturation humidity). This system allows for precise, steady and reproducible control of h2o deficit conditions.nine In the well-watered handling, none of the lines showed discernible staining for oxalate oxidase activity at whatsoever location within the apical 12 mm of the root (data not shown). In contrast, when grown nether water-stressed weather, the lines showed diverse spatial patterns of increased oxalate oxidase action (Fig. 1). Except for lines M162W, B73 and P39, all the temperate lines exhibited oxalate oxidase activity within the apical 3 mm region (as previously observed for FR69713), with some lines showing more pronounced staining than other lines. In addition, all the temperate lines showed oxalate oxidase activity in the basal region (beyond 6 mm from the apex). The three mixed ancestry lines also showed increased oxalate oxidase activeness in both the apical and basal regions. In contrast, the tropical lines showed several diverse patterns of oxalate oxidase action: CML247, CML277, CML322, CML333, NC350 and NC358 showed staining in both the apical few mm as well as the basal region, Tzi8 showed staining only in the apical region, CML 228 showed staining only in the basal region, whereas CML52, CML69,CML103,Ki11 and Ki3 showed no oxalate oxidase activity throughout the apical 12 mm. It is not unexpected that the tropical lines show a broader range of responses as they have wider variability within their pedigrees and contain higher levels of diversity than temperate maize.21
To ostend that the varied oxalate oxidase staining observed in the apical region of the root growth zone among the lines did not result from differential penetration of the staining solution, the apical 1.5–iii mm region of a subset of 10 lines was stained subsequently sectioning to let direct access of the solution to the tissues. The results were consistent with those observed in the intact roots (data non shown).
The NAM parents as well showed large variation in the response of primary root elongation to water stress, ranging from 24% (in NC358) to 47% (in P39) of the elongation observed in the corresponding well-watered controls (Fig. 2). To evaluate whether the response of root elongation was associated with the occurrence of oxalate oxidase action in either the apical 3 mm or the basal region of the growth zone, the oxalate oxidase activity in the different regions was scored as described in Tabular array S1. The results showed that the relative maintenance of root elongation nether water stress did not correlate with the occurrence of oxalate oxidase staining in either the upmost or basal regions (R two values were ≤ 0.ane).
Effigy ii. Relative maintenance of primary root elongation in the maize NAM parental lines during 48 h after transplanting to vermiculite at a water potential of -1.half-dozen MPa. The results are calculated as a percentage of well-watered controls; the well-watered and h2o-stressed root elongation data are presented in Effigy S1. Values are means ± SE of n = 13–25. Analysis of variance (PROC GLM, SAS version ix.three; SAS Institute) was used to compare the means among lines in each treatment. Least pregnant differences (LSD) for P values of 0.05 and 0.01 are shown. Experiments were repeated with a subset of x lines to confirm consistency of the root growth response.
The involvement of oxalate oxidases in biotic stress tolerance is common to different cereal species.22 Therefore, to investigate whether increased oxalate oxidase action in the root growth zone under water stress is a conserved response in cereals, nosotros examined a range of various rice lines. Rice was chosen because of known variation in response to water stress and because of the availability, for future studies, of RNAi lines for all of the oxalate oxidases nowadays in rice (J Leach, personal communication). X lines representing the diversity of rice (five japonica, four indica and i aus line) and known to accept contrasting water utilise efficiency parameters23 , 24 were selected for assay. Still, none of the lines showed any staining for oxalate oxidase activity in the apical few mm of the root under water-stressed conditions (Fig. 3). Interestingly, while the japonica lines besides exhibited no or marginal staining beyond 6 mm from the apex, the indica and aus lines consistently exhibited limited staining in this region. It should be noted, however, that we have not characterized the dimensions of the growth zone in the rice primary root under either well-watered or water-stressed conditions, and it is possible that the staining in the basal region was beyond the zone of prison cell elongation. The rice lines exhibited greater variation in the response of primary root elongation to water stress than that observed in maize (Fig. four). The least inhibited rice line was Cypress, which maintained 56% of the elongation of the well-watered command, whereas the poorest line (Moroberekan) showed but 22% maintenance of root elongation. There was no correlation between the occurrence of staining for oxalate activity in the basal region and the response of root elongation to water stress (R ii = 0.005; staining scores are shown in Table S1).
Figure iii. Oxalate oxidase activity determined past oxalate-dependent oxidation of 4-chloro-ane-naphthol in 12-mm apical segments of water-stressed principal roots (due north = 8–15) of diverse rice lines. Roots were harvested 48 h afterwards transplanting to vermiculite at a water potential of -one.2 MPa. Note that rice has a relatively thin primary root, resulting in less hydraulic contact with the vermiculite growth media compared with maize. Therefore, the rice seedlings were grown at a higher h2o potential than was used for maize. Other growth conditions and measurement procedures were as described in Figure 1.
Figure iv. Relative maintenance of principal root elongation in diverse rice lines during 48 h subsequently transplanting to vermiculite at a water potential of -1.ii MPa. The results are calculated as a percentage of well-watered controls; the well-watered and water-stressed root elongation data are presented in Figure S2. Values are ways ± SE of northward = xiii–18. Statistical analysis was conducted equally described in Figure 2; least pregnant differences (LSD) for P values of 0.05 and 0.01 are shown.
Taken together, the maize and rice results suggest that oxalate oxidase-mediated mechanisms are involved in regulating the growth response in the upmost region of h2o-stressed primary roots only in some maize lines and are not involved in any of the rice lines tested. Although a correlation between the occurrence of increased oxalate oxidase activeness and root growth maintenance under water deficit conditions was not apparent, information technology should be emphasized that the results exercise not necessarily imply that the maize and rice lines that lack an oxalate oxidase response also lack the response of increased apoplastic ROS levels in the apical region of the growth zone.13 Oxalate oxidase might not be a major contributor to apoplastic H2O2 product in these lines, and increased ROS levels could be achieved by increased activeness of other ROS-producing enzymes. These culling hypotheses could be tested by measuring apoplastic ROS levels in the rice and contrasting maize lines nether water stress atmospheric condition. The relevance of increased oxalate oxidase activeness to the response of root elongation under water stress tin can exist examined past manipulating oxalate oxidase activeness and documenting the effects on processes regulating root elongation. In a following paper, transgenic maize lines overexpressing oxalate oxidase25 volition be utilized for this purpose. The finding that maize has considerable genetic diversity in the response of oxalate oxidase activity, too as elongation, in h2o-stressed roots could be useful not only in physiological studies but also in convenance programs to meliorate root growth traits under water deficit conditions.
Supplementary Material
Additional material
Acknowledgments
We thank Dr. Jan Leach (Colorado State University) for supplying seed of the diverse rice lines. The study was supported by the Partitioning of Establish Sciences, the Interdisciplinary Plant Group and an Undergraduate Research Internship to H.J.T from the College of Agriculture, Nutrient and Natural Resource, University of Missouri.
Disclosure of Potential Conflicts of Interest
No potential conflicts of interest were disclosed.
Footnotes
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