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Rice Type I Phytochrome Regulates Hypocotyl Elongation in Transgenic Tobacco Seedlings

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Rice Type I Phytochrome Regulates Hypocotyl Elongation in Transgenic Tobacco Seedlings Proc. Natl. Acad. Sci. USA Vol. 88, pp. 5207-5211, June 1991 Botany Rice type I phytochrome regulates hypocotyl elongation in transgenic tobacco seedlings (light regulation/transgenic plants/plant development/growth regulation) AKIRA NAGATANI*, STEVE A. KAYt, MARIA DEAKt, NAM-HAI CHUAt, AND MASAKI FURUYA* *The Laboratory of Plant Biological Regulation, Frontier Research Program, RIKEN Institute, Hirosawa 2-1, Wako City, Saitama, Japan 351-01; and tThe Laboratory of Plant Molecular Biology, The Rockefeller University, 1230 York Avenue, New York, NY 10021-6399 Communicated by Winslow R. Briggs, February 11, 1991 ABSTRACT We have examined the biological activity of cDNAs from Arabidopsis thaliana (13) and tobacco (S.A.K., rice type I phytochrome (PI) in transgenic tobacco seedlings. M.D., and R. Kern, unpublished data). Thus, we have The progeny offour independent transformants that expressed operationally designated a molecular form of phytochrome the rice PI gene segregated 3:1 for shorter hypocotyl length that is light-labile and most abundant in dark-grown tissue as under dim white light (0.04 W/m2). By contrast, this pheno- type I phytochrome (PI) and one that is much less abundant type was not observed either in the dark or under white light and relatively stable irrespective oflight conditions as type II at higher intensity (6.0 W/m2). This suggests that the pheno- phytochrome (12, 14, 15). type is dependent not only on light but also on light intensity. It is possible to express a cloned phytochrome gene as well The increased light sensitivity cosegregated with the kanamy- as its mutant forms in transgenic plants. As previously cin-resistance marker as well as with the rice PI polypeptides, proposed (4), one can expect either to induce a dominant indicating that this phenotype is directly related to the expres- negative phenotype with a mutant molecule or to create an sion of the transgene. The transgenic plants showing short exaggerated phenotype by overexpression. This kind of hypocotyls exhibited a reduced growth rate throughout the experimental system can be readily used to probe functional elongation period, and the resulting shorter hypocotyl length domains of the introduced phytochrome. Such a system will was attributable to shorter epidermal cell length but not to also be useful in assigning distinct or overlapping roles for reduced cell number. Furthermore, successive pulse irradia- different types of the photoreceptor. Recently, we (16) and tions with red light elicited short hypocotyls similar to those two other groups (17, 18) have overexpressed a monocot PI obtained under dim white light, and the effect was reversed by gene in a transgenic dicot background. The introduced PI immediate far-red light treatment, providing a direct indica- showed normal Pr/Pfr photoconversion and was light-labile. tion that the phenotype is caused by biologically active rice PI. Several resulting phenotypes were also observed; Keller et Therefore, the far-red-absorbing form ofthe introduced rice PI al. (17) and Boylan and Quail (18) noted semidwarfism and appears to regulate the hypocotyl length of the transgenic dark green leaves, whereas we observed altered patterns of tobacco plants through endogenous signal-transduction path- endogenous Cab gene expression (16). However, the rela- ways. This assay system will be a powerful tool for testing the tionship between these phenotypes and the introduced phy- biological activity of introduced phytochrome molecules. tochrome molecules has remained unclear. To investigate the utility of this approach further, we have Phytochrome is a regulatory photoreceptor that plays a generated several transgenic tobacco lines overexpressing central role in linking external light signals to developmental rice PI. To assess the effects of the overexpression, we have responses in plants (1, 2). One of the underlying mechanisms designed an assay for hypocotyl length in transgenic tobacco of these developmental responses is the modulation of pat- seedlings. Using this assay, we have extended the previous terns of gene expression (3), and phytochrome has been studies by demonstrating that the short-hypocotyl phenotype shown to regulate the expression of many plant genes (4, 5). is not only dependent upon light intensity but also regulated An understanding of the molecular mechanism of phy- by the introduced rice PI. In addition, we have shown that tochrome action in vivo is therefore essential to elucidating rice PI influences hypocotyl length by altering cell length but the complex processes of plant growth and development. not cell number. Phytochrome is a soluble chromoprotein consisting of an apoprotein (monomer, 118-125 kDa) covalently linked to a linear tetrapyrrole (6) and is located in the cytoplasm in vivo MATERIALS AND METHODS (7). Phytochrome is synthesized in the dark as the red light Plant Materials. Tobacco plants (Nicotiana tabacum cv. (Amax = 666 nm)-absorbing form (Pr), which is physiologically Xanthi) were transformed with the construct containing rice inactive. Absorption of red light by Pr converts the molecule PI cDNA fused to the cauliflower mosaic virus (CaMV) 35S to the far-red light (Amax = 730 nm)-absorbing form (Pfr), promoter as described (16). The transformants, CR and CO, which is the biologically active conformation, and subse- which showed the highest rice PI mRNA accumulation quent irradiation of Pfr with far-red light converts the mol- among several independent transformants, were used in the ecule to the Pr form (8). Phytochrome responses are therefore present study. Preparation of the tobacco transgenic plants elicited by red light and attenuated by far-red light. BN1 and BD1 (cv. SR1), which overexpress rice PI, have Immunological studies have indicated that more than one been described (16). Control transgenic tobacco plants p69 type ofphytochrome exists in oat (9, 10) and in pea (11). More and 4C (cv. Xanthi) were transformed with constructs car- recently, this has been demonstrated at the molecular level rying the CaMV 35S promoter fused to the chloramphenicol by microsequencing of divergent pea phytochrome polypep- acetyltransferase (CAT) gene or 83-glucuronidase (GUS) tides (12) and by cloning of the divergent phytochrome gene, respectively. Primary transgenic plants were desig- The publication costs of this article were defrayed in part by page charge Abbreviations: CaMV, cauliflower mosaic virus; PI, type I phy- payment. This article must therefore be hereby marked "advertisement" tochrome; Pfr, far-red-absorbing form of phytochrome; Pr, red- in accordance with 18 U.S.C. §1734 solely to indicate this fact. absorbing form of phytochrome. 5207 Downloaded by guest on September 24, 2021 5208 Botany: Nagatani et al. Proc. Natl. Acad. Sci. USA 88 (1991) nated the Ro generation. The R1 and R2 seeds were obtained by (NH4)2SO4 precipitation (0.25 g/ml) and a 20-,u1 aliquot by selfing the R0 and R1 plants, respectively. Samples of was then subjected to NaDodSO4/PAGE. The proteins in the seeds from individual plants were first tested for kanamycin gel were electrophoretically blotted onto nitrocellulose mem- resistance by germinating the seeds on agar plates containing brane and stained with the anti-rye phytochrome monoclonal the antibiotic; seed populations that showed 3:1 segregation antibody (mAR14), which stained rice but not tobacco phy- for kanamycin resistance were used. tochrome (16), and the anti-pea PI monoclonal antibody Growth Conditions. For hypocotyl length determination, (mAP5), which stained tobacco PI but not rice PI (16), as the seeds were sown on 0.5% agar plates containing 0.1x described (21). The extraction procedures were carried out Murashige and Skoog salt mixture (19). The plates were kept under dim green safe light. under continuous white light (6.0 W/m2) for 2 days to induce seed germination and then subjected to the light treatments RESULTS for 5 days except where otherwise stated. To check the kanamycin resistance of the young seedlings after the light Segregation of the Short-Hypocotyl Phenotype Under Dim treatment, plants were transferred to 0.8% agar plates con- White Light. As described in our previous paper (16), we taining kanamycin (0.1 mg/ml) and Murashige's minimal could not observe a clear morphological phenotype in mature organics medium (20) after the light treatment and grown for plants of BN1 and several other transgenic tobaccos that 10-14 days at 250C under continuous white light. For immu- accumulated high levels of rice PI. In these previous exper- noblot analysis, young plants were transferred to soil and iments the SR1 tobacco cultivar was used as the transgenic grown for about 1 month under a 12 hr/12 hr light/dark cycle host. By contrast, the new transgenic lines, such as CR and in a growth cabinet (Koitotron KG-206HL-D, Koito, Tokyo) CO, which were derived from the Xanthi cultivar, clearly at 25TC. The plants were then dark-adapted for 3 days before showed shorter stem length and dark green leaves when harvest to increase the amount of phytochrome. grown under light/dark cycles (Fig. 1). However, these Light Sources. White light (6.0 W/m2) for inducing germi- phenotypes were less clear under continuous white light nation and growing plants on the agar plate was from white (A.N., unpublished data), suggesting that these phenotypes fluorescent tubes (FL20SS-W/18, Toshiba, Tokyo). Dim are dependent on the ambient light intensity. To investigate white light (0.04 W/m2) was obtained by attenuating the white this phenomenon we chose to examine young transgenic light with three layers of filter paper (3 MM Chr, Whatman). seedlings rather than mature plants, since the morphological Red light (0.4 W/m2) and far-red light (0.8 W/m2) were variations observed among individual mature plants were obtained from two fluorescent lamps (red, same as ones for usually much greater than those in younger plants. In addi- white light; far-red, long-wavelength fluorescent lamp, tion, one can test larger numbers of individual plants in less FL20SFR74, Toshiba, Tokyo) filtered through one layer of time with young seedlings.
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