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How Plants Sense and Respond to Environmental Stimuli

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How Plants Sense and Respond to Environmental Stimuli COMMENTARY Up, down, and all around: How plants sense and respond to environmental stimuli John Z. Kiss* Department of Botany, Miami University, Oxford, OH 45056 lthough plants are essentially support the hypothesis originally pro- sessile in nature, these organ- posed by Darwin and Darwin (1) that isms are very much in tune circumnutation had an internal driving with their environment and are force and regulating apparatus but add Acapable of a variety of movements. This support to the idea that oscillatory may come as a surprise to many non- movements in plants are directly cou- botanists, but not to Charles Darwin, pled to gravity sensing. who had a strong interest in plant biol- The present study reported in PNAS ogy during his multifaceted career. Al- (6) builds on the previous 2003 paper though it is one of his lesser known (7) in several interesting ways. The hy- works, Charles Darwin, along with his pothesis that the SCR protein in morning son Francis, published a fascinating glory is necessary for the differentiation book in 1880 entitled The Power of of the endodermis and gravity responses Movement in Plants (1). The Darwins in stems was supported by complemen- Fig. 1. Drawing from The Power of Movement in studied in great detail the two broad Plants (1) that illustrates the oscillatory movements tation tests for P. nil Scr (PnSCR) using categories of plant movements: the tro- (i.e., circumnutation) of the shoot of a young seed- the scr mutant of Arabidopsis. They also pisms (directed growth in response to ling of Brassica. The experiment was performed found that mutation of PnSCR causes external stimuli) and nastic movements over a period of 10 h and 45 min, and tracings were abnormal shoot circumnutation by (movements in response to stimuli, but of the shoot tip as viewed from above. studying gravitropism in wild-type morn- the direction is independent relative to ing glory, a morning glory scr mutant, the stimulus source). Examples of tro- and a transgenic Arabidopsis line with pisms include gravitropism, directed cells. In roots, the gravity-perceiving the mutant scr gene. In addition, other growth in response to gravity (2), and statocytes are located in the central col- Arabidopsis mutants that have the phototropism, growth in response to umella cells of the root cap, whereas in endodermis but with abnormal statolith light (3). Nastic movements include the stems, these statocytes are found in a movement (e.g., sgr2 and zig͞sgr4; ref. dramatic leaf movements of the Venus layer of cells adjacent to the vascular 10) were defective in the oscillatory flytrap after a touch stimulus and the tissue and are termed endodermal cells movements. The results of these studies less dramatic (but more ubiquitous) (Fig. 2). Both columella and endoder- and the various control experiments ‘‘sleep movements,’’ in which the leaves mal cells have dense amyloplasts (i.e., clearly demonstrate that the SCR gene of some plants (e.g., bean plants) move starch-filled plastids), called statoliths, regulates both circumnutation and grav- to a different position at night. The itropism in both Arabidopsis and morn- Darwins also studied oscillatory move- ing glory, thus clearly linking these two ments (also termed circumnutation; Fig. The SCR gene processes. 1), in which plants rotate around a cen- So it seems that the Darwins (1) may tral axis during their growth. Almost all regulates circumutation not have been right on this issue. How- plant parts exhibit this movement, but ever, the results of some experiments vines show an exaggerated circumnuta- and gravitropism in (11) on the space shuttle Columbia tion (4, 5). To date, it is unclear would no doubt have heartened Charles whether these oscillatory movements are Arabidopsis and Darwin. Sunflower seedlings were used an endogenous nastic movement or morning glory. in these experiments because these whether they are coupled to and depend plants exhibit a vigorous circumnutation on gravitropism. Although the Darwins (see Movie 1, which is published as sup- (1) were among the first to address porting information on the PNAS web that move in response to gravity (8). these issues, they have been most re- site). Brown and coworkers (11) studied cently considered by Kitazawa and co- Hatakeda et al. (7) found that a starch- 4-day-old seedlings in microgravity and workers (6) in a recent issue of PNAS. less mutant (thus, with small statoliths) found that 93% of these plants circum- The initial observations by this group of Arabidopsis that had reduced grav- nutated compared with 100% of the (6) published in a previous paper (7) itropism also exhibited a decreased cir- ground control. The circumnutation of suggested that there was a link between cumnutation. Additionally, another the spaceflight seedlings had a reduced circumnutation and gravitropism be- Arabidopsis mutant (scr for scarecrow) amplitude and period compared with cause an agravitropic mutant of the lacking an endodermis that was agrav- the ground plants. Nevertheless, the Japanese morning glory (Pharbitis nil) itropic in stems had an even more se- spaceflight study seemed to be definitive also was defective in circumnutation. vere lack of circumnutation. [A bit of The 2003 paper also reported on a se- background: the SCR gene belongs to a ries of gravitropic mutants in the plant gene family that encodes putative tran- Conflict of interest statement: No conflicts declared. Arabidopsis thaliana. Those mutants scription factors required for asymmetric See companion article on page 18742 in issue 51 of volume were deficient in the early steps of grav- cell divisions that are essential for 102. itropism because they had defects in endodermal differentiation in roots and *E-mail: [email protected]. their statocytes, or gravity-perceiving shoots (9).] Thus, these results do not © 2006 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0510471102 PNAS ͉ January 24, 2006 ͉ vol. 103 ͉ no. 4 ͉ 829–830 Downloaded by guest on September 29, 2021 the reduced amplitude and period re- ported (11). However, in the space ex- periments, some of the plants studied developed from seeds planted in orbit by the astronauts. Although their studies do not distinguish the results obtained from plants that first developed on the ground from those plants that were completely grown in microgravity, one must assume that most of these seed- lings exhibited circumnutation because 93% of the total plants had these oscil- latory movements. Based on the evidence to date, is there more support for the endogenous model of Darwin and Darwin (1) or the hypothesis that suggests that circumnu- tation depends on gravitropism most Fig. 2. Diagram of a root (a) and stem (b)ofArabidopsis to illustrate the regions of gravity perception. (a) Within the root cap at the apex, some cells develop into the gravity-sensing columella cells (yellow), recently advocated by Kitazawa et al. which are the statocytes. These cells contain amyloplasts (arrows) that function as statoliths and move in (6)? Clearly, there is strong support for response to the direction of the gravity (toward bottom). (b) The stem consists of an epidermal layer (Ep), the latter hypothesis provided for by the a cortical zone (C), an endodermal layer (En), and vascular tissue (VT). The endodermal cells (En; yellow) elegant study with multiple molecular are the statocytes with amyloplasts (arrows) functioning as statoliths. Ref. 6 suggests that the endodermal approaches outlined in ref. 6 and the cells also play an important role in circumnutation. previous studies from this group that used more structural methods (7). As a space biologist, I hope there will be op- and provides strong evidence that periodic that the differences are caused by plant portunities to confirm and extend these growth oscillations (i.e., circumnuta- species differences. Alternatively, experiments by using the microgravity tions) persist in the absence of signifi- Kitazawa and coworkers (6) propose environment aboard orbiting spacecraft cant gravitational accelerations. Thus, that because in these spaceflight experi- as a unique research tool (13). these results are in conflict with the ments (11, 12) the sunflower seedlings study reported by Kitazawa et al. (6). were germinated on the ground, the Maria Palmieri and Richard E. Edelmann as- How do we reconcile these two reports plants sensed gravity before and during sisted in the preparation of the figures. I thank and two hypotheses about the relation- the launch. Thus, the oscillatory move- Roger P. Hangarter for providing Movie 1 and ship between gravitropism and circum- ment was established on the ground, Richard C. Moore and Jack L. Mullen for help- nutation? One unsatisfying suggestion is and then circumnutation continued at ful comments on the manuscript. 1. Darwin, C. & Darwin, F. (1880) The Power of N., Miyazawa, Y., Hoshino, A., Iida, S., Fukaki, H., Benfey, P. N. & Tasaka, M. (1998) Plant J. 14, Movement in Plants (John Murray, London). H., Morita. M. T., Tasaka, M., et al. (2005) Proc. 425–430. 2. Blancaflor, E. B. & Masson, P. H. (2003) Plant Natl. Acad. Sci. USA 102, 18742–18747. 10. Morita, M. T. & Tasaka, M. (2004) Curr. Opin. Physiol. 133, 1677–1690. 7. Hatakeda, Y., Kamada, M., Goto, N., Fukaki, H., Plant Biol. 7, 712–718. 11. Brown, A. H., Chapman, D. K., Lewis, R. F. & 3. Correll, M. J. & Kiss, J. Z. (2002) J. Plant Growth Tasaka, M., Suge, H. & Takahashi, H. (2003) Venditti, A. L. (1990) Plant Physiol. 94, 233–238. Regul. 21, 89–101. Physiol. Plant. 118, 464–473. 12. Brown, A. H. & Chapman, D. K. (1984) Science 4. Brown, A. H. (1993) Plant Physiol. 101, 345–348. 8. Kiss, J. Z. (2000) Crit. Rev. Plant Sci. 19, 551– 225, 230–232. 5. Larson, K. C. (2000) Am. J. Bot. 87, 533–538.
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