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The primer sequences for the target and reference genes are listed in Supplementary Table S1. The areas of the individual cells were measured using ImageJ, and the number of ER bodies in each cell was counted manually.

For time-course analysis of ER body number and size in dehydration-stressed plants, GFP fluorescence was observed in petiole samples under an LSM confocal laser-scanning microscope Carl Zeiss, Jena, Germany using a nm diode laser line and a — nm detection band.

ABA was purified and quantified as described Preston et al. A clear extract was obtained by centrifugation, and the residues were re-extracted with extraction buffer without d 6 -ABA.

ABA-GE hydrolysis activity in microsomal fractions P as described above was assayed as described previously Watanabe et al.

Results are presented as means with SD from at least three independent experiments, unless otherwise noted. Linear regression analysis was applied to examine the correlation between RWC and time following stress treatment.

S2 ; Winter et al. However, few studies have examined the protein level of BGLU18, except for an experiment in which a BGLU18 transgene was ectopically expressed in transgenic Arabidopsis under a strong constitutive promoter Lee et al.

We examined the distribution of BGLU18 in the above-ground tissues mostly leaf blades and petioles of day-old Arabidopsis plants grown under normal conditions.

A Tissue distribution within true leaves. The upper panel shows the fractionation scheme and typical fluorescence images of subcellular fractions prepared from shoot extracts of GFP-h plants.

P1, P8, and P indicate pellets Ppt obtained after centrifugation at , , and g , respectively, and S indicates the supernatant Sup after centrifugation at g.

Analyses were conducted on a volume to volume basis. All experiments were repeated three times to confirm the reproducibility of the results, and one representative result is shown.

Therefore, both of these approaches demonstrated that under normal conditions, BGLU18 primarily occurs as a component of ER bodies and to a minor extent in the ER in leaf petioles.

Interestingly, before transient expression, we observed numerous spindle-shaped GFP spots in the leaf petiole and some in the leaf blade more in the midrib and edge and fewer in the lamina of GFP-h plants in the WT background Fig.

These ER bodies were evenly distributed on the adaxial and abaxial sides of the leaf. These observations indicate that the formation of these structures was not induced by bombardment but rather existed constitutively.

Because nai2 mutants lack constitutive ER bodies Yamada et al. The predominant distribution of BGLU18 in the leaf petiole suggests that this protein is physiologically important in this part of the leaf.

We therefore focused our analysis on leaf petioles. Tissue distribution of ER bodies in Arabidopsis leaves.

The first true leaf from a day-old plant grown under normal conditions was used. A Leaf portions subjected to fluorescence microscopic observation for GFP.

Leaf RWC decreased progressively Fig. S5 , thus supporting the validity of the stress treatment. Under dehydration treatment, the number of petiole ER bodies increased significantly 3.

These results demonstrate that in the leaf petiole, ER bodies not only exist constitutively, but their formation is also induced by these abiotic stresses.

Responses of ER bodies to abiotic stress in epidermal cells of Arabidopsis leaf petioles. A Effects of drought-induced dehydration stress on leaf relative water content RWC.

B Effects of dehydration stress on stress-responsive gene expression. Total RNA was extracted from the aerial parts of dehydration-stressed plants at the indicated time points.

Transcript levels of target genes were measured by RT—qPCR, normalized to those of SAND as a reference gene, and represented as values relative to the level at the start of stress 0 min , which was given a value of 1.

See Supplementary Fig. S5 for the results using other reference genes. To examine the responses of leaf petiole ER bodies to abiotic stress in further detail, we monitored the changes in their number and size over the course of a min dehydration treatment and following a period of recovery Fig.

Compared with control conditions, the number of ER bodies began to increase significantly within 30 min after the onset of stress and nearly doubled at 60 min, after which it returned to the original level 90 min and decreased further min Fig.

Coincident with the decline in the number of ER bodies, their average size was also reduced at 90 min and min Fig.

However, these ER bodies returned to their original state after recovery from dehydration, suggesting that the observed changes are part of the physiological response to stress treatment.

These results demonstrate that the ER in the leaf petiole undergoes dynamic changes, as evidenced by the reversible changes in ER body status, during dehydration stress and recovery.

Dynamic changes in leaf petiole ER bodies in response to drought-induced dehydration stress. A Representative time-course fluorescence images of leaf petiole epidermal cells of a GFP-h plant exposed to dehydration stress.

Aseptically grown plants were subjected to dry air for the indicated time period up to min. For recovery, stressed plants were restored to normal conditions and grown for an additional 18 h.

Two-dimensional sizes of individual ER bodies, as indicated by green spot areas, were determined as described in the Materials and methods.

To assess the relationship between BGLU18 and abiotic stress responses of leaf petiole ER bodies, we examined the status of ER bodies in the aln-1 mutant, which accumulates allantoin, since this purine metabolite activates BGLU18 and increases basal ABA levels under normal conditions Watanabe et al.

Consistent with previous findings, ABA-GE hydrolysis activity was highest in aln-1 , followed by the WT, and lowest in bglu18 , which we used as a background control given that BGLU18 is a member of a large enzyme family 47 members in Arabidopsis; Xu et al.

In the absence of stress, the resulting GFP-h aln-1 plants had significantly 3. These findings suggest that BGLU18 is a necessary component in the induction of ER body formation in the leaf petiole.

Immunoblotting was carried out as described in Fig. The histogram on the right shows the quantity of ER bodies in leaf petiole epidermal cells.

ER bodies are subcellular compartments that function in the temporary storage of certain BGLUs, such as BGLU23, which are released from the ER bodies upon stress to react with substrates stored separately in other compartments, such as vacuoles Yamada et al.

Therefore, we investigated whether abiotic stress affects the subcellular localization of BGLU Under stress conditions, mRFP signals, which overlapped fully with GFP signals under control conditions, had slightly diffused from major GFP spots ER bodies and became a bit more evenly distributed within the cell Fig.

This observation was supported by quantitative analysis of relative fluorescence intensities across the cell Fig. We also examined the distribution of endogenous BGLU18 in subcellular fractions obtained from dehydration-stressed plants by immunodetection.

Dehydration treatment increased the level of BGLU18 in the microsomal P fraction, albeit to a small extent, suggesting that stress affects the relative distribution of BGLU18 between ER bodies and microsomes consisting of ER membranes and lumen proteins Fig.

Right: line profile graphs showing relative pixel intensities for GFP green and mRFP red fluorescence upper, control; lower, stressed , which were line-scanned and quantified between the two white arrowheads in the merged panels on the left using ImageJ.

Biochemical fractionation followed by immunoblotting was performed starting with control plants and plants exposed to dehydration for 30 min.

Bar graphs below show the relative distribution of BGLU18 in the four fractions. ABA-GE hydrolysis activity in the WT was estimated to increase 3-fold when background bglu18 activity was subtracted from each condition.

Along with increasing enzyme activity, ABA levels significantly increased 2-fold in leaf petioles from stressed plants.

Consistent with the results described above Fig. In contrast, in nai , BGLU18 was distributed nearly evenly between the three fractions. These results indicate that the relatively high levels of BGLU18 in the microsomes of nai are due to its inability to form constitutive ER bodies.

Biochemical fractionation followed by immunoblotting analysis were performed as described in Fig. The experiments were repeated twice with similar results; results from one experiment are shown.

B ABA-GE hydrolysis activity upper and ABA levels lower in nai single and nai bglu18 double mutant plants under control conditions or exposed to dehydration for 30 min.

WT and bglu18 data used for comparison are from Fig. S7 , and compared these results with those for the WT and bglu18 single mutant Fig.

The nai plants showed the highest and the bglu18 plants the lowest ABA-GE hydrolysis activity under both normal and stress conditions Fig.

Introducing the bglu18 mutation into the nai background resulted in lower enzyme activity in the bglu18 nai double mutant compared with nai single mutant plants, suggesting that the nai mutation caused increased activity of BGLU18 and possibly other enzymes capable of degrading ABA-GE.

Along with enzyme activity, dehydration stimulated ABA accumulation by 5-fold in nai Fig. Under normal conditions, however, this increased enzyme activity did not lead to increased ABA levels in nai Neither the bglu18 single nor the bglu18 nai double mutant responded to dehydration stress treatment by increasing ABA levels, suggesting that de novo synthesis contributed little to increased ABA levels under our experimental conditions, as examined further below.

These results indicate that dehydration-responsive ABA production occurs in leaf petioles, a process mediated by BGLU18 and augmented by the loss of constitutive ER bodies, but this occurs only under stress conditions.

However, ABA levels increased slightly but significantly 1. ABA levels in leaf blades of the three genotypes exhibited a similar pattern to those in the petiole under both control and stress conditions, with slightly higher levels in leaf blades versus petioles Fig.

Taken together, these results indicate that BGLU18 is involved in an early stage of ABA accumulation not only in the petioles but also in the blades of dehydration-stressed leaves.

Effects of bglu18 and aba mutations on time-course changes in dehydration-induced ABA accumulation in leaf petioles and blades. The regulation of ABA accumulation is of fundamental importance for plant responses to abiotic stresses such as drought.

Although roots are the primary sites for sensing drought, there is evidence that the foliar production of ABA is independently required to elicit stress responses in leaves Holbrook et al.

However, in contrast to the extensive research on the multistep process of de novo ABA biosynthesis, far fewer studies have investigated the single-step hydrolysis of ABA-GE, which allows for quick ABA production.

Our results highlight the involvement of stress-induced ER dynamics in BGLUmediated ABA production, which has intriguing implications for the regulation of cellular ABA homeostasis during stress responses and adaptation.

Our results also shed light on the physiological functions of ER bodies, which remain to be fully explored. We first addressed the localization of BGLU18 in leaves at the tissue and subcellular levels.

BGLU18 was originally reported to be localized to the ER of leaf protoplasts based on a constitutive overexpression study Lee et al.

However, the enzyme was subsequently identified as a major component of ER bodies whose formation was induced in wounded cotyledons Ogasawara et al.

ER bodies that are constitutively present but limited to specific epidermal cells of leaf blades were recently identified and contained BGLU18 Nakazaki et al.

Here, we showed that this enzyme is present at higher levels in leaf petioles than in leaf blades, where it is predominantly, but not exclusively, localized to the ER bodies of epidermal cells Figs 1 , 2.

In addition, the current findings, together with those of Nakazaki et al. ER bodies increase in number in response to mechanical wounding in Arabidopsis cotyledons and leaves Matsushima et al.

Wound-inducible ER bodies, together with constitutive ER bodies, probably play a defensive role against biotic stresses such as herbivory and pathogenesis Sherameti et al.

Due to the known role of BGLU18 in ABA metabolism, we investigated whether ER bodies in leaves respond to abiotic stress conditions, which had not been examined previously.

In a pattern similar to the wounding response, the number of ER bodies in leaf petioles increased significantly in response to drought-induced dehydration stress, osmotic stress, or high salinity Fig.

Thus, dynamic changes in ER body status constitute a general stress response in Arabidopsis. Nevertheless, the changes in leaf petioles occurred over a much shorter period 30—60 min for dehydration and 12 h for osmotic and salt stress; Figs 3 , 4 than the time required for wounding responses in leaf blades 44—66 h; Matsushima et al.

In addition, the dehydration response of ER bodies in stressed cells was reversed following the removal of stress Fig. These differences might reflect the distinct roles played by ER bodies whose formation is induced upon dehydration and wounding, that is, in abiotic versus biotic stress responses.

Given our observations in leaf petiole tissues, we were interested in exploring whether abiotic stress-induced dynamic changes in ER body status were physiologically relevant to BGLU18 function.

We examined the effect of allantoin on ER body dynamics, as this ER-related purine metabolite activates BGLU18 and enhances basal ABA levels, while the inability to produce allantoin results in hypersensitivity to drought in Arabidopsis Watanabe et al.

Both endogenously accumulated resulting from the aln mutation and exogenously applied allantoin caused an increase in leaf petiole ER bodies in the absence of stress Fig.

How allantoin induces such ER dynamics remains to be elucidated. In contrast, under our experimental conditions, neither enzyme activity nor ABA levels were altered in the bglu18 mutant exposed to the same stress treatment.

Notably, upon exposure to dehydration, the size of ER bodies decreased following a transient increase in their numbers Fig. We tested this possibility using an ER body-deficient nai mutant.

Similarly, Lee et al. This idea was further supported by our time-course comparison of dehydration-induced ABA accumulation in leaves among genotypes, as the bglu18 mutant did not exhibit the early ABA accumulation that was observed in the WT Fig.

Conversely, the aba mutant showed slightly but significantly earlier ABA production in response to dehydration, even though de novo ABA synthesis is largely impaired in this mutant.

These results strongly suggest that the rapid activation of BGLU18 is responsible for the early ABA accumulation that precedes de novo biosynthesis, which might occur via a mechanism involving ER dynamics at the organellar level this study and post-translational regulation at the molecular level Lee et al.

The physiological significance of ABA production in the epidermal cells of leaf petioles remains to be addressed.

Our results suggest that ABA-GE hydrolysis plays a part in an early stress response to generate ABA, which might contribute to activation of the ABA biosynthetic pathway through positive feedback regulation Xiong et al.

Such feedback regulation would involve the translocation of ABA from BGLUcontaining epidermal cells to vascular parenchyma cells, where the genes for ABA biosynthetic enzymes are primarily expressed Koiwai et al.

The thin, stalk-like structure of the leaf petiole may be favorable for the translocation of ABA since epidermal tissues surround the vascular tissues in closer proximity in petioles compared with leaf blades.

However, this enzyme was recently proposed to act as a myrosinase to produce defense compounds from glucosinolate substrates in response to herbivory Nakazaki et al.

Given that ER bodies in leaves respond to both abiotic and biotic stress Matsushima et al. Since BGLU18 is physically separated from its substrates i.

ABA-GE and indole glucosinolates under normal conditions, the two distinct activities are probably regulated by the physiological process by which each substrate becomes available under stress conditions: as noted above, dehydration-induced ABA production might involve stress-activated transport of ABA-GE into the ER from the apoplast or vacuoles Lee et al.

If this scenario is accurate, BGLU18 in leaf petioles might also be involved in defense against biotic stress, as it is in leaf blades.

Changes in the relative transcript levels of stress-responsive genes during the course of drought-induced dehydration.

Genotyping and phenotyping of the bglu18 nai double mutant. Table S2. Validated method for phytohormone quantification in plants. Frontiers in Plant Science 5 , Google Scholar.

A re-examination of the relative turgidity technique for estimating water deficit in leaves. Australian Journal of Biological Sciences 15 , — Vacuolar transport of abscisic acid glucosyl ester is mediated by ATP-binding cassette and proton-antiport mechanisms in Arabidopsis.

Plant Physiology , — The Plant Cell 14 , — A hydraulic signal in root-to-shoot signalling of water shortage.

The Plant Journal 52 , — Extracellular beta-glucosidase activity in barley involved in the hydrolysis of ABA glucose conjugate in leaves.

Journal of Experimental Botany 51 , — Abscisic acid uridine diphosphate glucosyltransferases play a crucial role in abscisic acid homeostasis in Arabidopsis.

Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells.

The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. The occurrence of abscisic acid and abscisyl-beta-d-glucopyranoside in developing and mature citrus fruit as determined by enzyme immunoassay.

Plant Physiology 82 , — A proteinase-storing body that prepares for cell death or stresses in the epidermal cells of Arabidopsis. Herman E , Schmidt M.

Endoplasmic reticulum to vacuole trafficking of endoplasmic reticulum bodies provides an alternate pathway for protein transfer to the vacuole.

Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying. Journal of Experimental Botany 53 , — Tissue-specific localization of an abscisic acid biosynthetic enzyme, AAO3, in Arabidopsis.

Intertissue signal transfer of abscisic acid from vascular cells to guard cells. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid.

Cell , — Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci.

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