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First published online November 6, 2003; 10.1104/pp.103.027490 Plant Physiology 133:1820-1830 (2003) © 2003 American Society of Plant Biologists Impaired Induction of the Jasmonate Pathway in the Rice Mutant hebiba1Biologisches Institut II, Albert-Ludwigs-Universität Freiburg, Schänzlestrasse 1, 79104 Freiburg, Germany (M.R., A.K., P.N.); Lehrstuhl für Pflanzenphysiologie, Ruhr-Universität Bochum, 44793 Bochum, Germany (A.M., E.W.W.); and Hitachi Advanced Research Laboratory, Hatoyama, Saitama 350-0395, Japan (M.F.)
The elongation of rice (Oryza sativa) coleoptiles is inhibited by light, and this photoinhibition was used to screen for mutants with impaired light response. In one of the isolated mutants, hebiba, coleoptile elongation was stimulated in the presence of red light, but inhibited in the dark. Light responses of endogenous indolyl-3-acetic acid and abscisic acid were identical between the wild type and the mutant. In contrast, the wild type showed a dramatic increase of jasmonate heralded by corresponding increases in the content of its precursor o-phytodienoic acid, whereas both compounds were not detectable in the mutant. The jasmonate response to wounding was also blocked in the mutant. The mutant phenotype was rescued by addition of exogenous methyl jasmonate and o-phytodienoic acid. Moreover, the expression of O. sativa 12-oxophytodienoic acid reductase, an early gene of jasmonic acid-synthesis, is induced by red light in the wild type, but not in the mutant. This evidence suggests a novel role for jasmonates in the light response of growth, and we discuss a cross-talk between jasmonate and auxin signaling. In addition, hebiba represents the first rice mutant in which the induction of the jasmonate pathway is impaired providing a valuable tool to study the role of jasmonates in Graminean development.
Plant growth and development have to be tuned with the environment. This requires an intensive interaction between signaling triggered by external stimuli and endogenous growth regulators. As a consequence of their photosynthetic lifestyle, plants have evolved a very efficient cross-talk between light signaling and growth. Changes in the content of plant hormones have been frequently invoked as effector system for the light responses. For instance, local depletion from auxins in response to blue light (Went, 1928  ), inhibition of the terminal steps in GA biosynthesis triggered by red light (Campell and Bonner, 1986), or a light-induced block of brassinosteroid synthesis (Li et al., 1996) are classical examples for light-triggered responses in synthesis or distribution of growth regulators. For the cross-talk of light with GAs as well as with brassinosteroids, potential targets have been recently identified in pea (Pisum sativum). For instance, light induced the down-regulation of a small G protein, Pra2, that is required for the activation of a cytochrome P450 C-2 hydroxylase involved in brassinolide synthesis (for review, see Clouse, 2001), whereas at the same time through a different pathway, light stimulates the 2 -hydroxylation of GA1 to GA8, thus removing the active GA from the elongating tissue (O'Neill et al., 2000).
The rice (Oryza sativa) coleoptile represents a useful system to study the interaction between light, hormonal signaling, and a photomorphogenetic response: Aerially grown coleoptiles respond to light by an inhibition of growth. The response is swift and exclusively based on an inhibition of cell elongation concomitant with a block of basipetal auxin transport from the perceptive site in the coleoptile tip to the major site of cell elongation in the basal region (Furuya et al., 1969
The Response to Light Is Inversed in hebiba Coleoptiles In etiolated seedlings of the wild type, the coleoptile is long and the mesocotyl is short (Fig. 1A). Under the red-light treatment used for the screen, the coleoptiles are short and pierced by the expanding primary leaves. In contrast, in irradiated seedlings homozygous for the mutated hebiba allele, the coleoptile was long, and the primary leaves were still hidden inside reminiscent of etiolated wild-type seedlings (Fig. 1A). However, etiolated seedlings of the mutant displayed a characteristic phenotype with short, bent coleoptiles and prolonged mesocotyls.
Adult mutant plants were characterized by excessive leaf growth (Fig. 1B). The leaves were not erect but tended to hang downwards and even creep along the soil provoking the name "hebiba" (Japanese for "snake leaf") for this mutant. The leaves, although growing vigorously, were light green in color in contrast to the dark-green leaves of the wild-type plants raised in the same phytochamber (Fig. 1C). This change in color was accompanied by a 4-fold reduction in the ratio of chlorophyll a to chlorophyll b (data not shown). The mutant flowered earlier than the wild type: After transfer to inducing short day, flowering in the mutant initiated after 25.3 ± 0.6 d (n = 20) as compared with 31.8 ± 0.8 d (n = 20) in the wild type. Although the mutant plants flowered, the seeds were not filled and therefore were not viable. So far, through seven generations raised under a broad range of climatic conditions, not a single fertile plant homozygous for the mutant allele could be observed. As shown by Table I, reciprocal crosses with wild-type plants show that fertility can be restored by cross-pollination with wild-type pollen indicating male sterility. When seeds from heterozygotes are propagated in the field, the mutation is conveyed to about two-thirds of the following generation matching the predicted frequency under the assumption that the viability of heterozygous embryos is not impaired. The offspring of selfed heterozygotes segregates into about a quarter of seedlings where the mutant phenotype is manifest and three-quarters that are indistinguishable from the wild type. These data are matching with the predicted outcome under monogenic Mendelian inheritance with complete dominance of the wild-type allele over the mutant allele under complete male sterility of homozygous mutant plants.
Mutant coleoptiles are short in the dark and long in the light (Fig. 1A). This means that the light response of growth is reversed in hebiba. The presence of a clear dark phenotype suggests that hebiba is not a photoreceptor mutant or a photomorphogenetic mutant in sensu strictu—a "blind" mutant should not have a phenotype in the absence of light. Thus, it is more probable that the mutant is impaired in the light-triggered effector system. Classical studies (Furuya et al., 1969
As compared with the wild type, etiolated mutant coleoptiles are characterized by a slightly reduced content (by about one-third as compared with the wild type) of indolyl-3-acetic acid (IAA). In both wild type and mutant, IAA decreases somewhat during irradiation with red light at a comparable time course (Fig. 3A). After 2 h of red light, about 40 to 50 pmol g-1 fresh weight was reached, irrespective of whether the samples originated from wild type or mutant or from the basal or the apical halves of the coleoptile. Interestingly, no significant auxin gradient could be detected between apical and basal halves either in the wild type or in the mutant, either in etiolated or in irradiated coleoptiles.
To understand the growth stimulation in the mutant despite a reduced content of auxin, we assayed the auxin sensitivity and responsiveness of growth in a classical segment assay (Fig. 3B). When the dose response curve of auxin-dependent coleoptile growth was determined, the amplitude of the response was found to be dramatically elevated. This was especially impressive for superoptimal concentrations of auxin when growth in the wild type was not induced, whereas it proceeded at almost the maximal velocity in the mutant. In contrast, the threshold and the maximum of the curve were reached at the same concentrations of auxin as in the wild type. Thus, there are no indications for an increase of auxin sensitivity in the mutant, whereas the responsiveness of the auxin response is amplified. When the content of ABA was measured (Fig. 3C), the apical halves of wild type and mutant were found to be more or less identical (around 20 pmol g-1 fresh weight). During irradiation, the ABA content decreased to less than one-half of the original value, but this decrease was almost identical between wild type and mutant. The situation was different when the basal halves (the center of growth activity) were analyzed: The ABA content was found to be 2.5 times higher in the basal regions of etiolated mutant coleoptiles as compared with the corresponding wild-type sample. Again, ABA content decreased in response to red light, which was more pronounced in the mutant. However, the relative difference (with more than 2-fold increased ABA in the basal region of the mutant) was maintained. The decreased content of auxin and, more strikingly, the increased content of ABA in the growth zone correlates well with the repressed growth activity of mutant coleoptiles that are kept in the dark. The light-induced decrease of auxin qualitatively correlates with the reduced growth in the wild type (although a reduction by 30% is certainly not sufficient to account for the dramatic inhibition of growth). However, it can obviously not be responsible for the stimulation of growth in the mutant. On the other hand, the pronounced decrease of ABA (an inhibitor of coleoptile growth) in the basal zone of the mutant would be consistent with the stimulation of growth by light. In contrast, the decrease of ABA observed in the wild type cannot account for the observed inhibition of growth in response to red light. Whereas the light responses of auxin and ABA were found to be of relatively minor amplitude, the analysis of JA and its precursor OPDA revealed dramatic responses in the wild type that were completely absent in the mutant. In the wild type, JA was substantially and rapidly stimulated by a factor of 10 to 20 (Fig. 4A). The increase was faster and more pronounced in the apical region of wild-type coleoptiles and was somewhat slower in the basal region. Interestingly, OPDA, a precursor of JA, was found to increase transiently before the strong increase in JA content (Fig. 4B). The peak of OPDA content was observed at 30 min, i.e. concomitant with the inhibition of growth. In the basal region, where growth activity is centered, the OPDA peak was more conspicuous and disappeared concomitantly with the increase of JA content. In the apical region, the OPDA peak became only weakly manifest and the temporal sequence between (transient) OPDA increase and (stable) JA increase was somewhat smaller than in the basal region.
Irrespective of coleoptile region or time of irradiation, neither OPDA nor JA could be detected in coleoptiles of the hebiba mutant (Fig. 4, A and B). Interestingly, already before irradiation, certain basal levels of OPDA and jasmonate were clearly present in the wild type, whereas they could not be detected in the mutant (Figs. 4, A and B, insets). These findings can be summarized in three statements: (a) Red light triggers the jasmonate pathway—the amplitude of this response is in the range of about 1 order of magnitude and thus conspicuously exceeds the fluctuations in the content of other hormones, such as IAA or ABA. (b) The light response of the jasmonate pathway is completely absent in the hebiba mutant. In contrast, the other hormones tested exhibit a light response that is fairly similar to the wild type. (c) The hebiba mutant not only lacks a response of the jasmonate pathway, it does not contain either JA or its precursor, OPDA.
The light response of the jasmonate pathway could be due to a light-specific defect in the signaling toward jasmonate synthesis (i.e. very upstream), or it could be caused by impaired expression or activity of enzymes involved in JA synthesis (i.e. downstream). To distinguish between these possibilities, we tried to trigger the JA pathway by a standardized wounding treatment. In the wild type, this treatment led to a rapid, extreme induction of JA (to more than 6,000 pmol g-1 fresh weight; Fig. 5A) and a 30-fold increase of OPDA (Fig. 5B) in the wild type. In hebiba coleoptiles, neither OPDA nor JA could be detected. This indicates that the mutation affects the general response of the JA pathway and is therefore not specific for light signaling.
The hebiba mutant cannot trigger the jasmonate pathway in response to light or wounding (Figs. 4 and 5). It exhibits an inverse growth response to light (Fig. 1A), and male sterility (Table I). To understand whether this phenotype is related to the blocked jasmonate induction, we tested whether the mutant can be rescued by exogenous methyl jasmonate. Coleoptiles of wild type and mutant were cultivated on various concentrations of methyl jasmonate. In one experimental set, the coleoptiles were kept in complete darkness (Fig. 6A). Alternatively, they were irradiated with red light between d 4 and 5 after sowing and then returned to the dark (Fig. 6B).
In the dark and in the absence of methyl jasmonate, the mutant showed the characteristic inhibition of coleoptile growth that was accompanied by hyper-trophic elongation of the mesocotyl (Fig. 6A). Upon increasing concentrations of methyl jasmonate, the mutant phenotype progressively disappeared (data not shown). At 100 nM of methyl jasmonate, mutant and wild-type seedlings were found to be of identical morphology with a fully elongated coleoptile and a stunted mesocotyl. After irradiation and in the absence of methyl jasmonate, the mutant phenotype was most conspicuous with fully elongated coleoptiles of about 30 mm length that were still covering the primary leaves (Fig. 6B), whereas in the wild type, the coleoptiles were short (less than 10 mm) and pierced by the primary leaves. The mutant phenotype was more persistent to lower concentrations of methyl jasmonate as compared with growth in complete darkness. However, at 100 nM of methyl jasmonate, mutant and wild type had become indistinguishable with short, stunted coleoptiles that had been opened by the primary leaves. To test, whether the phenotype could be rescued by precursors of jasmonate, seedlings of wild type and mutant were fed with exogenous OPDA and linolenic acid. We were able to obtain a complete rescue of the mutant phenotype in the dark by 10 µM of OPDA (Fig. 6A). In the case of red light, the mutant phenotype disappeared in a dose-dependent manner: With an increasing concentration of OPDA, coleoptiles shortened progressively, and the primary leaves penetrated the coleoptile, but it was not possible to reach the complete inhibition of growth that was observed in the wild type (Fig. 6B). In our experimental setup, it was not possible to rescue the phenotype by addition of exogenous linolenic acid. Although we observed a slight decrease of coleoptile length for 100 µM of linolenic acid in irradiated mutants, but not in the wild type, we failed to approximate the wild-type phenotype by raising the concentration of linolenic acid (we tested 200 µM, 500 µM, and 1 mM) due to a general inhibition of growth in both wild type and mutant.
To test the induction of the jasmonate pathway by red light in the hebiba mutant on the level of gene expression, we investigated the red-light response of O. sativa 12-oxophytodienoic acid reductase (OsOPR), an early gene of jasmonate synthesis (Sobajima et al., 2003
To test, whether the male sterility of the mutant could be rescued by exogenous jasmonate, flowering was triggered by transfer of adult plants to inductive short days, and 5 µM methyl jasmonate was administered through the roots at different days after the transfer. Negative controls that were treated by water did not develop a single viable seed. The same was observed when methyl jasmonate was administered later than d 7 after the transfer to inductive short days. In contrast, fertility could be restored when methyl jasmonate was added from the day of transfer to inductive short days. Summarizing, we observe that the mutant fails to induce jasmonate synthesis, irrespective of the inducing stimulus (light or wounding). The light response of mutant coleoptiles can be rescued with respect to normal photomorphogenesis by exogenous methyl jasmonate and partially by OPDA in a dose-dependent manner. Moreover, the fertility of adult mutant plants can be restored by exogenous methyl jasmonate.
The rice mutant hebiba was isolated from a screen for plants defective in photomorphogenesis as a putative "red-blind" candidate. This assumption was made because in this mutant coleoptile, elongation was not inhibited by irradiation with red light. However, growth of mutant coleoptiles was reduced in darkness. Thus, the phenotype cannot be explained in terms of a photoreceptor mutation. Compared with the wild type, the mutant exhibits a mirrored light response (blocked elongation in the dark, stimulated elongation in the light). This situation allows investigating the role of hormonal changes for the growth response to light. We therefore analyzed the response of auxin, the major player in the control of coleoptile elongation, and ABA, an important negative regulator of coleoptile elongation (Hoffmann-Benning and Kende, 1992 ; Gianì et al., 1998). We measured the content of these hormones separately in the basal and apical halves to see whether transport or gradients of these hormones exist and are disturbed in hebiba. From the observed inversion of growth regulation by light, we expected to find high levels of auxin (accompanied by low levels of ABA) in the mutant under conditions when it is low in the wild type and vice versa. To our surprise, neither the observed changes in the content of IAA nor those of ABA were consistent with the growth phenotype of hebiba. The level of IAA in the mutant was reduced in etiolated seedlings, but it did not increase after red-light irradiation as would be expected from the stimulation of growth. On the contrary, IAA decreased even further, which was quite similar to the response in the wild type (Fig. 3A). Intriguingly, the amount of ABA was regulated down after red-light irradiation in both the apical and basal regions in hebiba, but this response was observed in the wild type as well (Fig. 3C). Thus the light response of IAA and ABA cannot account for the stimulation of growth that is observed in the mutant.
Because auxin-induced growth of coleoptile segments can be inhibited by exogenous jasmonate (Ueda et al., 1994 Our result that the biosynthesis of jasmonate is triggered by red light in wild-type rice was confirmed by the finding that the expression of OsOPR mRNA was induced in the wild type upon irradiation with red light, whereas it was not induced in hebiba (Fig. 7). Moreover, OsOPR mRNA is expressed on a low level in the mutant. Nevertheless, the phenotype can be rescued by OPDA, suggesting that the gene product, although expressed at a low level, is functional and can convert its substrate, given that it is provided by the enzymes acting upstream. This supports the conclusion from the complementation assays with jasmonate and OPDA that the HEBIBA gene must be located either upstream of OPR in the biosynthetic pathway or in a component regulating the entire biosynthesis of jasmonate. We do not think that OPR itself is impaired in its activity—it is expressed (although at a low level). The low expression of OPR in the mutant and the impaired induction by red light speaks preferentially for a general defect in the regulation of the pathway rather than for a mutation that inactivates one of the synthesizing enzymes. However, it cannot be excluded that the low expression of OPR originates from feedback mechanisms of the product to the synthesizing machinery that is secondarily impaired in consequence of the very low level of jasmonate in this mutant. To approach this problem further avoiding artifacts caused by potential differences of penetration in feeding assays, we launched a broad-scale analysis, where the fatty-acid profiles are compared between wild type and mutant.
The male sterility of hebiba, a typical symptom of deficient jasmonate biosynthesis or signaling (Xie et al., 1998 The failure of hebiba mutants to trigger the jasmonate pathway in response to wounding (Fig. 5) along with the finding that even a basic level of jasmonate and OPDA can be observed in the wild type before irradiation (Fig. 4, A and B, insets) suggest that the mutant is not only impaired in the pathway conveying the light signal to jasmonate biosynthesis but possibly in the biosynthetic pathway itself (or in a regulative event relatively close to biosynthesis). We are presently investigating whether enzymes of the jasmonate pathway are impaired in the mutant before irradiation.
Thus through the hebiba mutant, we uncovered a novel role of jasmonate in photomorphogenesis complementing the classical functions of this hormonal pathway such as wounding (for review, see León et al., 2001
How could the jasmonate pathway feed into the regulation of growth and cause a down-regulation of cell elongation in response to red light? In a classical segment elongation assay, Ueda et al. (1994 This suggests a scenario, where red light through the jasmonate pathway would down-regulate the auxin responsiveness of growth. In fact, when a dose response curve is measured for etiolated segments of wild type and hebiba (Fig. 3B), it reveals a dramatically elevated amplitude, whereas threshold and peak of the curve are found at the same concentrations as in the wild type. Thus, the complete absence of jasmonate in the mutant (in contrast to a certain basic level in the wild type; see Fig. 4, A and B, insets) is correlated with an increased responsiveness of auxin-induced growth (at a basically identical auxin sensitivity). The observation that before irradiation, the level of IAA was reduced in hebiba, whereas at the same time, the amount of ABA in the basal one-half of mutant coleoptiles was increased (Fig. 3, A and C) indicates that the jasmonate constitutively produced in the wild type acts in a negative feedback loop on the synthesis of ABA and probably indirectly slightly stimulates auxin synthesis.
Is there a mechanism that could explain a reduced responsiveness to auxin after activation of the jasmonate pathway? Recent findings about ubiquitin-related processes in phytohormonal signal transduction (for review, see Frugis and Chua, 2002 Using the hebiba mutant as a tool, we want to study the cross-talk and antagonism of auxin and jasmonate signaling in other auxin-mediated processes as well and to uncover the mechanism responsible for this antagonism. We recently launched the identification of the HEBIBA gene to get further insight into the cross-talk between auxin and jasmonate. At the same time, our mutant is a powerful tool to analyze signaling events triggered by jasmonate in rice such as pathogen attack.
Plant Material The rice (Oryza sativa) hebiba mutant was obtained in a japonica background (rice cv Nihonmasari) and has been propagated independently in two sites in northern Italy (Almo Semi, Mortara) and Japan (Hokuriku Experimental Station, Niigata). The mutant is male sterile, such that it has to be maintained through the heterozygotes. For each plant, small seed aliquots are checked separately to define the genotype of the population. An isogenic sister line homozygous for the wild-type allele was used as reference throughout the study.
The screen was performed under 52 µmol m-2 s-1 of red light (660 nm) originating from fluorescent tubes (FL-20S, Re66, Toshiba, Tokyo) and isolated by a color filter (3 mm thickness; acrylight K5-102, Mitsubishi Rayon, Tokyo) combined with a dispersion filter (3 mm thickness; acrylight K5-001E, Mitsubishi Rayon) installed in a phytotron (Koitotron, Koito, Tokyo). The light sources for red light (660 nm) and green safelight (550 nm) used in the photobiological studies are described in detail by Mohr et al. (1964
Starting material for the screen was a collection of independent mutant lines in a japonica background (rice cv Nihonmasari) that were screened for impaired growth inhibition under continuous red light. From each mutant line, aliquots of 20 seeds were cultivated for 3.5 d at 25°C according to Nick et al. (1994
In the time-course experiment for red-light irradiation, 6-d-old seedlings were transferred into a red-light field (3.4 mmol m-2 s-1) at 25°C for 0, 30, 60, or 120 min, respectively. In the wounding experiment, 6-d-old seedlings were wounded by squeezing them every 0.5 mm along the axis of the coleoptile with a ribbed forceps. Before harvest, they were kept in darkness for 30, 60, and 120 min, respectively. After the respective treatment, the coleoptiles were harvested immediately in green safelight (550 nm).
For the cultivation of seedlings in solutions of different concentrations of methyl jasmonate (Sigma-Aldrich), OPDA (synthesized by Axel Müller according to Laudert et al. [1997 For the auxin dose response curve, decapitated coleoptile segments of 5.5 mm were incubated in distilled water for 1 h to deplete them from internal auxin. After the depletion, they were incubated in IAA solutions of different concentrations (wild type: 0 nM, 50 nM, 5 µM, 10 µM, 100 µM, and 200 µM; hebiba: 0, 5 nM, 50 nM, 500 nM, 5 µM, 10 µM, 20 µM, 100 µM, and 500 µM) for 1 h. The growth increment was plotted against the concentration of IAA. The whole procedure was performed in green safelight; during depletion and incubation, the segments were rotated on a topover-shaker.
To determine the time course of growth inhibition by light, the growth rate of intact coleoptiles that had been precultivated in complete darkness for 6 d was determined either in continuing darkness or after transfer to red light. To measure the growth rate of dark-grown coleoptiles, they were monitored at different time intervals up to 4 h with an infrared-sensitive video camera (Grundig Electronic, Grundig, Nürnberg, Germany) in front of an infrared light source. By means of a time-lapse control, the infrared source was switched on only during the 1-min interval, when the image was recorded. A long-term experiment showed that the growth of these infrared-irradiated coleoptiles was identical to that of coleoptiles that were cultivated in continuous darkness. In a parallel experiment, dark-grown coleoptiles were transferred to the red light used for the hormonal measurement, and the length increment was determined optically at 0, 30, 60, and 120 min after the transfer.
For each sample, about 150 to 300 mg of plant material was analyzed. The material was transferred to a glass tube and immediately covered with 1 mL of methanol containing 30 pmol of H2-labeled IAA, ABA, and JA, and 10 pmol of H2-labeled OPDA as standard. After the addition of 1 mL of diethylether, the sample was incubated for 30 min at 50°C in a water bath. Afterward, the solvents were completely evaporated under vacuum.
Levels of the different hormones were determined as described by Müller et al. (2002
For the time course of OsOPR induction in response to red-light irradiation, etiolated seedlings grown for 6 d were transferred into the red-light field used for the phytohormonal analysis for the indicated time intervals. Coleoptiles were directly transferred to liquid nitrogen during harvest, and total RNA was extracted with the RNeasy kit (Qiagen, Hilden, Germany) according to the protocol of the producer. Ten micrograms of total RNA of each sample was loaded on a 1.2% (w/v) agarose gel. After electrophoresis, RNA was blotted onto a positively charged nylon membrane following standard protocols (Sambrook et al., 1989
We thank Prof. Hisakazu Yamane (University of Tokyo) for kindly providing OsOPR cDNA and Dr. Osamu Yatou (Hokuriku National Agricultural Experiment Station, Niigata, Japan) for providing seed material. Received May 25, 2003; returned for revision June 27, 2003; accepted August 31, 2003.
1 This work was partially supported by the Forschungsschwerpunkt "Molekulare Analyse der Phytohormonwirkung" of the Deutsch Forschungsgemeinschaft (to A.M., E.W., and P.N.), by Hitachi Advanced Research Laboratory (grant no. B2023), by the Japanese Program for Promotion of Basic Research Activities for Innovative Biosciences (to M.F.), and by the Volkswagen-Foundation Nachwuchsgruppen-Programme (to P.N. and M.R.).  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.027490. * Corresponding author; e-mail michael.riemann{at}biologie.unifreiburg.de; fax 49-761-203-2612.
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