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High Temperature Promotes Auxin-Mediated Hypocotyl Elongation in Arabidopsis

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High Temperature Promotes Auxin-Mediated Hypocotyl Elongation in Arabidopsis Proc. Natl. Acad. Sci. USA Vol. 95, pp. 7197–7202, June 1998 Plant Biology High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis WILLIAM M. GRAY*, ANDERS O¨ STIN†,GO¨RAN SANDBERG†,CHARLES P. ROMANO‡, AND MARK ESTELLE*§ *Department of Biology, Indiana University Bloomington, IN 47405; †Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Science, S-901 83 Umeå, Sweden; and ‡Cereon Genomics LLC, Cambridge, MA 02139 Edited by Bernard O. Phinney, University of California, Los Angeles, CA, and approved April 9, 1998 (received for review September 24, 1997) ABSTRACT Physiological studies with excised stem seg- Ethylene both positively and negatively regulates hypocotyl ments have implicated the plant hormone indole-3-acetic acid elongation. In darkness, ethylene inhibits elongation, but at (IAA or auxin) in the regulation of cell elongation. Supporting least under some conditions in the light, ethylene promotes evidence from intact plants has been somewhat more difficult elongation (8). Precisely how this complex array of hormonal to obtain, however. Here, we report the identification and controls is integrated with regulation by light and other characterization of an auxin-mediated cell elongation growth environmental factors is poorly understood. We have identi- response in Arabidopsis thaliana. When grown in the light at fied an additional environmental control of hypocotyl growth. high temperature (29°C), Arabidopsis seedlings exhibit dra- We find that high temperature promotes dramatic hypocotyl matic hypocotyl elongation compared with seedlings grown at elongation in light-grown Arabidopsis seedlings. This temper- 20°C. This temperature-dependent growth response is sharply ature-induced growth response depends on indole-3-acetic reduced by mutations in the auxin response or transport acid (IAA or auxin). pathways and in seedlings containing reduced levels of free The ability of exogenous auxin to promote cell elongation in IAA. In contrast, mutants deficient in gibberellin and abscisic excised stem and hypocotyl segments has been studied exten- acid biosynthesis or in ethylene response are unaffected. sively (9). This strong growth-promoting property of auxin Furthermore, we detect a corresponding increase in the level provided the basis for its identification as the first known plant of free IAA in seedlings grown at high temperature, suggesting hormone by Went nearly 70 years ago. The role of auxin in that temperature regulates auxin synthesis or catabolism to regulating cell expansion in intact plants is somewhat less clear, mediate this growth response. Consistent with this possibility, however, because application of exogenous auxin often does high temperature also stimulates other auxin-mediated pro- not stimulate elongation. The inability of exogenous auxin to cesses including auxin-inducible gene expression. Based on stimulate prolonged cell expansion led to the suggestion that these results, we propose that growth at high temperature auxin plays little if any role in regulating plant growth by cell promotes an increase in auxin levels resulting in increased elongation (10). More recent studies, however, have found a hypocotyl elongation. These results strongly support the con- correlation between endogenous auxin levels and stem andyor tention that endogenous auxin promotes cell elongation in hypocotyl length (4, 11, 12). Furthermore, by using a contin- intact plants. uous auxin infusion system, Yang et al. (13) were able to demonstrate that exogenous IAA can promote prolonged stem Plant growth and development are regulated by both external growth in pea seedlings. Our findings that temperature- environmental factors, such as light quantity and quality, and induced hypocotyl elongation (i) correlates with an increase in by a set of endogenous regulators collectively known as the IAA levels, (ii) depends on the auxin transport and response phytohormones. In many instances, these two sets of deter- systems, and (iii) is diminished in transgenic seedlings con- minants interact with one another. For example, phytohor- taining reduced levels of free IAA strongly support the mones mediate many of the stress responses that facilitate contention that endogenous auxin is capable of promoting cell adaptation to environmental changes. One of the most studied elongation in intact plants. examples of this occurs during periods of drought stress, when the phytohormone abscisic acid mediates stomatal pore clo- MATERIALS AND METHODS sure, resulting in reduced transpirational water loss (1). The Arabidopsis hypocotyl is a useful model for investigating Plant Material and Growth Conditions. The Arabidopsis the regulation of plant growth. Hypocotyl elongation in Ara- thaliana etr1–1, ein2–1, aba-1, and ga4–1 mutant lines were bidopsis is the result of regulated cell expansion that is under obtained from the Arabidopsis Biological Resource Center at both environmental and hormonal controls (2). In the absence Ohio State University and have been described previously of light, seedlings undergo skotomorphogenic development. (14–17). det2–1 seed was the generous gift of J. Chory (18). The cotyledons remain closed, an apical hook is formed, and The auxin response and transport mutants used in this study the hypocotyl becomes greatly elongated. Light induces the also have been described elsewhere (19–21). The aba-1 and photomorphogenic developmental program resulting in coty- ga4–1 mutations are in the Landsberg erecta background. ledon expansion, leaf development, the initiation of photosyn- Wild-type Landsberg erecta seedlings were used in experi- thesis, and limited hypocotyl growth. In addition to light, all of ments involving these two mutants. All other wild-type, mu- the known plant hormones have been implicated in the control tant, and transgenic lines used in this study are in the Columbia of hypocotyl elongation. Brassinosteroids, auxin, and gibberel- (Col-0) ecotype. Transgenic plants expressing the bacterial IAA–lysine synthase (iaaLys) gene originally were generated lins (GAs) promote hypocotyl growth, whereas cytokinins and in the RLD background with pMON690 as described (4, 22, abscisic acid (ABA) have growth inhibitory effects (3–7). 23). The 35s-iaaLys transgene then was backcrossed exten- The publication costs of this article were defrayed in part by page charge This paper was submitted directly (Track II) to the Proceedings office. payment. This article must therefore be hereby marked ‘‘advertisement’’ in Abbreviations: GAs, gibberellins; ABA, abscisic acid; IAA, indole-3- accordance with 18 U.S.C. §1734 solely to indicate this fact. acetic acid; GUS, b-glucuronidase; NPA, naphthylphthalamic acid. © 1998 by The National Academy of Sciences 0027-8424y98y957197-6$2.00y0 §To whom reprint requests should be addressed. e-mail: mestelle@ PNAS is available online at http:yywww.pnas.org. bio.indiana.edu. 7197 Downloaded by guest on September 26, 2021 7198 Plant Biology: Gray and Estelle Proc. Natl. Acad. Sci. USA 95 (1998) sively into Col-0. Expression of the iaaLys protein was con- destaining with 70% ethanol as described (25). To quantitate firmed by immunoblot analysis. As previously reported for GUS activity, crude extracts were prepared from the shoots of other plant species expressing this IAA-conjugating enzyme 9-day-old seedlings grown at 20°C or 29°C, and GUS activity (22), we found that the 35s-iaaLys Arabidopsis line used in this was assayed by using a spectrophotometric assay (26). Re- study contains a lower level of free (unconjugated) IAA than ported values are the average of at least four independent corresponding wild-type seedlings (see Table 2 below). Plants assays. harboring the SAUR-GUS and P. sativum pIAA4-GUS reporter genes were the gifts of P. Green (Michigan State Univ.) and A. RESULTS Theologis (Plant Gene Expression Center), respectively. The 35S-GUS reporter line CS6151 was obtained from the Arabi- High Temperature Promotes Hypocotyl Elongation in dopsis Biological Resource Center at Ohio State University. Light-Grown Seedlings. The effect of sustained high temper- Plants were grown under sterile conditions in vertical Petri ature on plant growth and development was examined by plates containing ATS nutrient media (19). Hormones and growing wild-type Arabidopsis seedlings at 29°C. Germination, auxin transport inhibitors were added after autoclaving. Plants growth, and development proceeded relatively normally at were grown in incubators at 20°C or 29°C under constant light 29°C with the plants progressing through the entire life cycle at an intensity of 85 mEm22 sec21. Data were collected from and producing viable seed. Development was slightly acceler- 9-day-old seedlings unless noted otherwise. ated at high temperature, with lateral roots and primary leaves Measurement of Hypocotyl and Cell Length. Hypocotyl initiating 1–2 days earlier than plants grown at 20°C. Plants lengths of 9-day-old seedlings were measured from shadow grown at 29°C also bolt, flower, and senesce significantly projections with a Simmon Omega variable condenser. For earlier than control plants (data not shown). In young seed- axr1–12 and naphthylphthalamic acid (NPA)-treated seed- lings, the most noticeable affect of high temperature was a lings, the cotyledons were excised to facilitate the measure- dramatic increase in hypocotyl and petiole length in light- ment of extremely short hypocotyls. Epidermal cell length was grown plants. The hypocotyls of wild-type seedlings
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