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(American Journal of Botany. 1999;86:1796-1800.)
© 1999 Botanical Society of America, Inc.

Dominant Wilty mutants of Zea mays (Poaceae) are not impaired in abscisic acidperception or metabolism1

Christopher D. Rock2,1 and Patrick P. F. Ng1

1 Department of Biology, Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong, China

Received for publication March 1, 1999. Accepted for publication June 4, 1999.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 LITERATURE CITED
 
Abscisic acid (ABA) is a plant hormone involved in growth, development, and stress adaptation. It acts via multiple pathways including rapid closure of stomatal pores by ion efflux from guard cells (thereby decreasing water loss) and by slower changes in gene expression. The Wilty2, Wilty3, and Wilty-2445 mutants are nonallelic members of a class of dominant mutants whose top leaves wilt when plants are subjected to drought conditions. We investigated the ABA responses of the Wi2 mutant by analysis of leaf transpiration rates and RAB17 (Responsive to ABA) gene expression. Wi2 leaves transpired less than those of wild-type siblings, but the slopes of Wi2 and wild-type ABA dose-leaf transpiration curves were identical, suggesting that Wi2 guard cell sensitivity to ABA is normal. Based on total RNA blot analysis, RAB17 transcripts in unstressed and drought-stressed Wi2 leaves were elevated relative to wild-type tissue. Wi2 ABA concentrations were also elevated relative to wild type in both unstressed and drought-stressed leaves. Similar to the Wi2 phenotype, Wilty3 and Wi-2445 mutants transpired less than their wild-type siblings and had normal ABA and ABA-conjugate levels, as measured by gas chromatography-mass spectrometry. Despite lower leaf transpiration rates, Wi2 mutants lost a greater percentage of fresh mass over time compared to the wild type. The previously characterized recessive mutant wilty1, which has a defect in vascular element development, also had reduced transpiration rates. It is concluded that the dominant Wi2, Wi3, and Wi-2445 mutants are not impaired in ABA metabolism or signaling. It is hypothesized, based on preliminary data, that the dominant mutants described here are impaired in vascular element development, analogous to the wilty1 mutant.

Key Words: ABA • abscisic acid • drought • gene expression • plant vascular development • transpiration


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 LITERATURE CITED
 
The sesquiterpene plant hormone abscisic acid (ABA) mediates a myriad of physiological processes in growth and development, including cell division, water use efficiency by closure of stomata, and gene expression during seed development and in response to environmental stresses such as chilling, salinity, drought, pathogen attack, and UV light (Zeevaart and Creelman, 1988 ; Chandler and Robertson, 1994; McCarty, 1995 ; Albinsky et al., 1998; Carrera and Prat, 1998 ; Leung and Giraudat, 1998 ; Wang et al., 1998 ). ABA is found in all plants, and the biosynthetic pathway from carotenoids through oxidative catabolism to phaseic acid or conjugation to ABA-glucose esters has been elucidated (see Koornneef et al., 1998 , for review).

ABA acts via multiple pathways, including rapid closure of stomatal pores by ion efflux from guard cells and slower changes in gene expression. Molecular genetic studies in the model organisms maize and Arabidopsis have resulted in the identification and cloning of ABA biosynthesis and signaling genes such as the carotenoid cleavage enzyme, protein phosphatases and kinases, transcription factors, and a subunit of farnesyl transferase (Schwartz et al., 1997 ; Bonetta and McCourt, 1998 ; Finkelstein et al., 1998 ; Ishitani et al., 1998; Koornneef et al., 1998; Luerssen et al., 1998 ; Sheen, 1998 ; Burbidge et al., 1999 ). However, our molecular understanding of ABA physiology is still fragmentary.

Wilty2, Wilty3, and Wi-2445 are nonallelic members of a class of EMS (ethyl methane sulfonate)-induced dominant mutants whose phenotypes are expressed beginning at the five-leaf stage as wilting of the top leaves whenever subjected to drought conditions (Neuffer, 1989, 1990 ; unpublished data). Under low stress conditions the mutants grow well and are not distinguishable from normal sibs. Homozygotes are viable but more extreme than heterozygotes. Wilty2 has been mapped to chromosome 3 (Neuffer, 1989 ). Because the wilty phenotype of these mutants is reminiscent of ABA biosynthesis and ABA signaling mutants, we investigated the ABA physiology of these mutants. We found that ABA metabolism, as well as guard cell and nuclear responses, appear normal in the mutants. We obtained preliminary evidence that these mutants may be defective in vascular element development, similar to the defect in the recessive wilty1 mutant (Postlethwait and Nelson, 1957 ).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 LITERATURE CITED
 
Seed stocks of Wi2 (Neuffer, 1989 ), Wi3 (Neuffer, 1990 ), and Wi-2445 were obtained from Prof. Gerry Neuffer, University of Missouri, Columbia, Missouri, USA. The pedigrees were: Wilty2 (40:220.1 x 201–15, Mo20Y/W23 x Wi2/+); Wilty3 (46:98–9 x 121–8 [M14 W23 wx/M14 wx x Mo20Y W23/Wi3] and 55:102 x 107–2 [B73 Wx x Wi3-1614/+; Mo17]); Wi-2445 (53:500 x 478–81 [Mo20Y W23 x (B73Ht/A632) M1/Wi-2445] and 51:600 x 553–32 [Mo20Y W23 x Wi-2419/+; A632]). The recessive mutant wilty1 (81–1123/1122–7) was obtained from the Maize Genetics Stock Center (University of Illinois, Urbana, Illinois, USA). Arabidopsis thaliana L. Heynh. seed stocks of Landsberg erecta wild-type (CS20), aba1-1 (CS21), abi1-1 (CS22), and abi2-1 (CS23) were obtained from the Arabidopsis Biological Resource Center (Ohio State University, Columbus, Ohio, USA).

Heterozygotes and wild-type siblings of Wi2, Wi3, and Wi-2445 were scored after the five-leaf stage in greenhouse-grown plants. The whole seventh to tenth emergent leaves (~25 cm in length) from wild-type or wilty plants were detached and used for leaf transpiration and mass loss experiments. Measurement of leaf transpiration rates in response to various concentrations of ABA fed through the transpiration stream was performed according to Raskin and Ladyman (1988) with modifications. Eight week-old greenhouse-grown wild-type or mutant (scored visually) leaves were cut under a solution of 0.1% (v/v) Tween 20 and the cut end introduced into a vial covered with parafilm into which a slit was cut. The vials contained 8 mL of water or various concentrations of (±) cis, trans-abscisic acid (Sigma, St. Louis, Missouri, USA). The leaves were placed in a growth chamber (Conviron, Winnipeg, Manitoba, Canada) at 23°C under 340 µmol photons·m-2·s-1 intensity illumination for 4–10 h, at which time the volume of water in the vial lost to transpiration was measured. The leaf areas were measured with a LI-COR 3100 (LI-COR, Lincoln, Nebraska, USA) leaf area integrator (Duke Univesity Phytotron, Durham, North Carolina, USA).

For mass loss experiments, detached leaves were placed on an analytical balance that was connected to the serial port of a personal computer, which recorded the mass every 2 s. The relative water loss was calculated as percentage of initial fresh mass as a function of time.

RNA blot analysis was as described in Rock and Quatrano (1996) . A 440 bp (base pair) PstI fragment of pMA12 (Gomez et al., 1988 ), kindly provided by Prof. Montserrat Pagès, Centre d'Investigació i Desenvolupament, C.S.I.C., Jordi Girona, Barcelona, Spain) was gel purified, random labeled with {alpha}-32P-dCTP (111 TBq/mmol, Amersham, Arlington Heights, Illinois, USA), and used to probe 10 µg/lane total RNA blots.

ABA determinations by enzyme-linked-immunoassay were as described by Bostock and Quatrano (1992) . Deveined leaves of mutant and wild-type siblings were weighed and either frozen in liquid nitrogen immediately (control) or subjected to a stream of warm air from a hair dryer until samples had lost 15% of their fresh mass. The samples were then incubated in the dark at room temperature in a plastic bag for 4 h, and frozen in liquid nitrogen. Samples were extracted repeatedly (four to six times) with 4 mL 80% (w/v) acetone containing 0.01% 2,6-di-tert-butyl-4-methylphenol and 0.25% (v/v) glacial acetic acid until no chlorophyll remained in the residue, and the extracts were pooled and dried in a Speed Vac (Savant, Holbrook, New York, USA). Before extraction, a 100-µL aliquot (330 Bq) of 3H-(±)ABA (2 TBq/mmol, Amersham) was added to each sample to correct for losses during purification.

ABA and ABA-conjugates were separated by reverse phase HPLC (Millipore, Milford, Massachusetts, USA) using a Novapak C18 10 x 0.4 cm column (Millipore). Injection was in 2 mL of 10% (v/v) ethanol, 0.25% glacial acetic acid. Elution was with a linear gradient of methanol from 10 to 60% in 20 min at a flow rate of 1.0 mL/min. UV absorbance of the eluate was monitored at 264 nm. ABA-conjugates were collected from 18.5 to 20.5 min, based on retention time of phaseic acid, which co-elutes with ABA-conjugates (Rock and Zeevaart, 1990 ). Phaseic acid was obtained from Dr. Sue Abrams, Institute of Plant Biotechnology, Saskatoon, Canada. The ABA fraction was collected from 23.2 to 25.2 min. Samples were dried in a Speed Vac and the ABA-conjugates fraction hydrolyzed with 2 mol/L NH4OH at 60°C for 2 h to yield free ABA. After evaporation to dryness, the ABA and ABA-conjugates fractions were methylated with ethereal diazomethane and aliquots subjected to quantification by gas chromatography-mass spectrometry (GC-MS). Recoveries were typically 50% for ABA.

Quantitation of ABA-Me by GC-MS was with a Finnegan (San Jose, California, USA) GCQ ion trap mass spectrometer interfaced with a Finnegan gas chromatograph. The column used for separation was a DB-5 capillary (30 m x 0.25 mm I.D., film thickness 1.0 µm; J&W Scientific, Rancho Cordova, California, USA) injected in splitless mode with He as the carrier gas (constant flow velocity of 40 cm/s). GC conditions were: oven temperature programmed to hold at 60°C for 1 min, followed by a linear gradient of 10°C/min to 275°C. ABA-Me eluted at 10'48'' trans-ABA-Me eluted at 11'13''. Phaseic acid eluted at 11'04''. Methane was used for the reagent gas for negative chemical ionization. The trap offset was 3 V, and the ion source temperature was 150°C to minimize fragmentation of the parent ions m/z = 278 for ABA-Me. Ion abundance of the molecular ion and two fragments of ABA-Me, m/z = 245 and m/z = 260 (Heath et al., 1990 ), was integrated over the peak area for quantitatition by interpolation with a standard curve from 62 to 1 pg ABA-Me (r = 0.996, N = 6).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
LITERATURE CITED
 
In order to determine whether the Wilty2 mutant is impaired in ABA perception, two functional assays, leaf transpiration and ABA-inducible gene expression, were performed. Figure 1 shows an ABA dose-response curve of leaf transpiration rates in Wilty2 and wild-type sibling leaves fed various concentrations of ABA through the transpiration stream. The results indicate that the Wilty2 mutants actually have significantly lower transpiration rates than wild-type leaves over the range of ABA concentrations tested (P < 0.02, Student's two-sided t test, equal variance assumed). The slopes of the log-linear dose-responses of Wi2 mutant and wild type are similar, suggesting that the sensitivities of the two genotypes to ABA are the same. Since there was no evidence that the response was saturated at extremes of ABA concentration in either genotype, it is not possible to conclude that the sensitivity to ABA is altered in the mutant.



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  		Fig. 1. ABA dose-response curve of leaf transpiration rates in wild-type ({diamondsuit}) and Wilty2 ({square}) siblings fed various concentrations of ABA through the transpiration stream for 10 h. Data points (± SE) are the average of 3–7 independent samples from one to three experiments

 
We extended our analysis of transpiration rates to include the other available dominant wilty mutants, Wi3 and Wi-2445, as well as the previously characterized recessive wilty1 mutant (Postlethwait and Nelson, 1957 ). After treatment with a moderately high (10-5 mol/L) concentration of ABA, all mutants showed lower transpiration rates than their corresponding wild-type sibs (Table 1). A statistical analysis of the data suggests the lower transpiration rates of the mutants are significant (Table 1). These results, taken together, suggest that the Wilty2 mutant, and probably the Wilty3 and Wi-2445 mutants, are not impaired in ABA perception leading to stomatal closure.


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  		Table 1. Transpiration rates of detached wilty1, Wilty-2445, and Wilty3 leaves in response to 10-5 mol/L ABA fed through the transpiration stream

 
To further characterize the Wilty2 mutant in terms of ABA responses, the transcript abundance of an ABA-inducible reporter gene, Rab17 (Gomez et al., 1988 ), in unstressed and water-stressed wild-type and Wilty2 leaves was determined by total RNA blot analysis. Furthermore, endogenous ABA was quantified from the same samples by enzyme-linked-immunoassay in order to determine whether a defect in ABA biosynthesis could contribute to the Wilty2 phenotype. The results are shown in Fig. 2. In wild-type leaves, Rab17 is induced by drought stress (Fig. 2A), as are ABA levels (Fig. 2C). However, in Wilty2 leaves, Rab17 is constitutively expressed in "unstressed" and drought-stressed leaves, and ABA levels are correlatively high in the same samples (Fig. 2A, C). These results suggest that ABA signaling leading to gene expression is not impaired in the Wilty2 mutant, nor is ABA biosynthesis impaired. Indeed, the evidence is consistent with the hypothesis that the mutant leaves are adapted to the wilty state, perhaps due to increased ABA biosynthesis and ABA-inducible gene expression.



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  		Fig. 2. Northern blot analysis of Rab17 expression in unstressed and 4-h drought-stressed wild-type (W.T.) and Wilty2 leaves, and quantitation of ABA in the same samples. (A) Autoradiograph of hybridized 32P-labeled pMA12 probe to the 0.9-kb Rab17 transcript. (B) Ethidium-bromide-stained formaldehyde-agarose gel of total RNA (10 µg), showing equal loading per lane. (C) Quantitation of ABA in aliquots of identical samples A and B by enzyme-linked immunoassay. Results are from one of two experiments with similar results.

 
To further characterize ABA metabolism in other wilty mutants, ABA and "bound" ABA-conjugates, most likely ABA-glucose ester (ABA-GE; Zeevaart and Creelman, 1988 ), were quantified by GC-MS in unstressed and 4-h drought-stressed leaves of Wilty-2445 and Wilty3 mutants and wild-type sibs. The results are shown in Table 2. The concentrations of ABA and ABA-GE were similar in mutant and wild-type siblings, both in unstressed and drought-stressed tissues. For the Wilty3 and wild-type genotypes, there was a two- and sixfold increase in ABA levels in response to 4-h drought stress, respectively. The wild-type Wilty-2445 siblings had relatively elevated ABA levels and did not increase their ABA concentrations in response to drought stress (Table 2). However, the unstressed samples had low recoveries of ABA (3 and 8%), and therefore the corrected amounts of ABA may be artifactually high (data not shown). All mutants and wild type also accumulated phaseic acid (data not shown). Taken together, these results establish that ABA metabolism is not impaired in the Wilty2, Wilty-2445 or Wilty3 mutants.


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  		Table 2. ABA and ABA conjugate levels (nmol/g fresh mass [±SE]) in Wilty-2445 and Wilty3 mutants and wild-type drought-stressed leaves

 
In order to address the mechanism of water loss by Wilty2 mutants, a leaf transpiration assay was performed on whole, detached leaves of wild-type and Wilty2 leaves grown under controlled (growth chamber) conditions. The results are shown in Fig. 3. A control transpiration experiment with the wilty Arabidopsis ABA-deficient aba1 and ABA-insensitive abi1 and abi2 mutants (Koornneef et al., 1998 ) is presented in Fig. 3A to validate the assay. Wilty2 mutant leaves lost a greater percentage of fresh mass over time than did leaves of wild-type siblings (Fig. 3B). This result is in apparent contradiction to previous results that show Wilty2 transpires less than the wild type (Fig. 1), yet is consistent with the wilty phenotype. We speculate that the reduced transpiration rates observed in all the wilty mutants (Table 1) may be due to the inability of mutant leaves to transport water efficiently. Postlethwait and Nelson (1957) showed that the wilty1 phenotype was due to delayed development of vascular elements. We have obtained preliminary evidence for this hypothesis by microscopic observation of cross-sectioned stems of Wilty2, Wi-2445, and Wilty3 mutants and wild-type plants that had been severed at the root-shoot interface and the stem placed in acid fuchsin stain for 30 min. Non-wilted lower (leaves 2–4) mutant leaves and all wild-type leaves took up the dye efficiently and stained the proto- and metaxylem elements, but the upper wilted Wi2, Wi-2445 or Wi3 leaves did not stain (data not shown). Thus, if water transport is reduced in the wilty mutants due to delayed xylem element development, this could affect the transpiration rates as measured by feeding solutions through the transpiration stream. Analysis of transpiration by upper and lower leaves of wilty mutants may corroborate this hypothesis.



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  		Fig. 3. Fresh mass loss from detached leaves of wild-type and wilty mutants of Arabidopsis and maize as a function of time. (A) Arabidopsis wild type ({diamondsuit}) and wilty mutants (aba1 [o], abi1 [], and abi2 [{diamond}]). Data points (± SD where shown) are the average of 3–7 replicates. (B) Maize wild type ({diamondsuit}) and Wi2 ({square}). Results are from one experiment, repeated once with similar results.

 
Conclusion
We have determined that the dominant wilty mutants Wi2, Wi3, and Wi-2445 are not impaired in ABA perception or metabolism, but may be affected in vascular element development. The dominant nature of the mutations lends itself to transposon tagging and cloning of the genes, which may in turn shed light on the molecular mechanism(s) of action of Wi2, Wi3, and Wi-2445.


   FOOTNOTES
 
1 C.D.R. thanks Ralph Quatrano for financial support, Pat Bedinger for help with maize fieldwork, Tom Phillipi for help with leaf area measurements, Theresa Terrazas and Bill Dickison for help with microscopy, and Gerry Neuffer for seed stocks and helpful discussions. We thank Regina Chak for performing Arabidopsis transpiration assays. This work was supported by NIH grants GM44288 to Ralph Quatrano and GM 14752 to C.D.R., and by a Competitive Earmarked Research Grant HKUST 6173/97M from the Hong Kong Research Grants Council to C.D.R. Back

2 Author for correspondence (phone [+852] 2358–8634; FAX [+852] 2358–1559; borock{at}ust.hk ). Back


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