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Role of Endodermal Cell Vacuoles in Shoot Gravitropism

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Role of Endodermal Cell Vacuoles in Shoot Gravitropism J Plant Growth Regul 2002) 21:113±119 DOI: 10.1007/s003440010047 Role of Endodermal Cell Vacuoles in Shoot Gravitropism Takehide Kato,1 Miyo Terao Morita,2 and Masao Tasaka2,* 1Department of Botany, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto, 606-8502, Japan 2Graduate School of Biological Sciences, Nara Institute of Science and Technology, Nara, 630-0101, Japan ABSTRACT In higher plants, shoots and roots show negative endodermis would function as statoliths, just as in and positive gravitropism, respectively. Data from roots. surgical ablation experiments and analysis of starch The study of the sgr2 and zig/sgr4 mutants pro- de®cient mutants have led to the suggestion that vides new insights into the early steps of shoot columella cells in the root cap function as gravity gravitropism, which still remains unclear. SGR2 and perception cells. On the other hand, endodermal ZIG/SGR4 genes encode a phospholipase-like and a cells are believed to be the statocytes that is, gravity v-SNARE protein, respectively. Moreover, these perceiving cells) of shoots. Statocytes in shoots and genes are involved in vacuolar formation or func- roots commonly contain amyloplasts which sedi- tion. Thus, the vacuole must play an important role ment under gravity. Through genetic research with in amyloplast sedimentation because the sgr2 and Arabidopsis shoot gravitropism mutants, sgr1/scr and zig/sgr4 mutants display abnormal amyloplast sedi- sgr7/shr, it was determined that endodermal cells are mentation. essential for shoot gravitropism. Moreover, some starch biosynthesis genes and EAL1 are important for the formation and maturation of amyloplasts in Key words: Shoot gravitropism; Endodermis; shoot endodermis. Thus, amyloplasts in the shoot Amyloplast; Vacuole; Mutant; Arabidopsis thaliana INTRODUCTION The physiology and cytology of the gravitropic response have been studied in various organs of Higher plants must adapt to particular environ- different plants. Studies indicate that several or- mental conditions to achieve optimal growth. Tro- ganelles and molecules play important roles in this pisms are important directed growth responses to response Kaufman and others 1995; Sack 1991). environmental conditions. When shoots are reori- The gravitropic response can be divided into at least ented, they bend upward to grow away from grav- four temporal steps: gravity perception, signal for- ity, whereas roots grow down towards gravity. The mation, signal transduction, and asymmetric cell gravitropic response enables leaves to ef®ciently elongation to induce bending Tasaka and others acquire light and roots to acquire water and various 1999). There are two major hypotheses regarding nutrients. plant gravitropism: the ``starch-statolith hypothe- sis'' states that amyloplast sedimentation in gravity sensing cells is a trigger event in the gravitropic Received: 16 October 2001/Accepted: 14 December 2001/ Online publication: 24 May 2002 reaction Kiss 2000; Sack 1991, 1997). In addition *Corresponding author: e-mail: [email protected] the ``Cholodny-Went Theory'' states that auxin is 113 114 T. Kato and others Figure 1. Shoot gravitropism in Arabidopsis thaliana. After in¯orescence stems are placed horizontally A), the stems begin to bend upward within 30 minutes, and the curvature reaches approximately 90 degrees in 90 minutes B). C)A part of transverse section of an in¯orescence stem in Arabidopsis showing a radial symmetrical pattern. A potential graviperceptive endodermal cell contains amyloplasts arrowheads). Ep, epidermis; Co, cortex; En, endodermis; St, stele. involved in differential cell elongation in gravitro- mutants can be categorized into two groups; one pism Firn and others 2000). group, including sgr3, 5 and 6, shows abnormal Many Arabidopsis mutants with aberrant shoot gravitropism only in in¯orescence stems, the other, and/or root gravitropism have been isolated, and including sgr1, 2, 4 and 7, shows abnormality both in the mutated genes have recently been cloned see in¯orescence stems and hypocotyls. This indicates recent reviews on this subject by Chen and others that the genetic regulation of gravitropism can be 1999; Firn and others 2000; Rosen and others 1999; slightly different in in¯orescence stems and hy- Tasaka and others 1999, 2001). In this paper, we pocotyls, even though the tissue and cellular concentrate on describing the mechanism of gravity structures involved in gravitropism are similar perception in shoots. Tasaka and others 1999, 2001). Although dicot in¯orescence stems curve in a short zone after gravistimulation, the region of gravity perception and response is broad in the ENDODERMAL CELLS FUNCTION AS elongation zone of shoots. This is shown by the fact GRAVITY PERCEPTION CELLS IN that every short fragment of an in¯orescence stem SHOOTS responded to gravity in physiological experiments Fukaki and others 1996a; Tasaka and others 1999; After vegetative growth of six to seven rosette Weise and others 2000). Moreover, the region of leaves, Arabidopsis in¯orescence stems bolt and gravity perception and response in hypocotyls also elongate in a straight, upward direction. When in- is broad in the elongation zone. ¯orescence stems are placed horizontally Figure The tissue structure of monocot shoots is some- 1A), they begin to bend within 30 minutes, and the what different from that of dicots. The stems of curvature reaches approximately 90 degrees in 90 grasses such as maize and oat also show negative minutes Figure 1B) Fukaki and others 1996a). gravitropism, but they curve only at a de®ned lo- Hypocotyls also exhibit negative gravitropism. Eti- cation called the pulvinus which is located just at olated hypocotyls elongate upward and bend neg- the base of the leaf and shows differential growth in atively when they are reoriented Fukaki and others response to gravity stimulation. However, interest- 1996a). ingly, the pulvinus does not elongate during de- Many mutants with abnormal shoot gravitropism velopment of the stem Collings and others 1998; have been isolated in Arabidopsis, including a series Kaufmann and others 1987, 1995). The coleoptile, of shoot gravitropism sgr) mutants. Seven indepen- an embryonic organ of grass plants, is a sheath- dent loci have been identi®ed by genetic analysis to shaped organ and the top part is more sensitive to relate to shoot gravitropism Fukaki and others gravity orientation, although the region responsible 1996b, 1998; Yamauchi and others 1997). Inter- for orientation covers the entire organ Sack 1991). estingly, all of these mutants show normal root Root tissues are easy to study microscopically via gravitropism, indicating that shoot gravitropism is microsurgical operations. Surgical ablation, or dis- genetically distinct from root gravitropism. The sgr ruption of the root cap by inserting a toxic gene Vacuoles Function and Shoot Gravitropism 115 under the control of the root cap speci®c promoter), However, the roots, which have columella cells has indicated that the root cap is important for root with normal amyloplasts, exhibit normal gravitro- gravitropism Juniper and others 1966; Tsugeki and pism. Thus, these observations suggest that the Fedoroff 1999). Additionally, laser ablation of col- amyloplasts in the endodermis of shoots and hy- umella cells has clearly demonstrated that columella pocotyls are essential for shoot gravitropism Fu- cells are essential for root gravitropism Blanca¯or jihira and others 2000). and others 1998). However, since it is dif®cult to Starch-de®cient mutants that store fewer or no observe and analyze living cells inside of shoots, we starch granules in amyloplasts, have been isolated. had little direct evidence indicating where gravity The starchless mutants show abnormal gravitropic perception occurs in shoot tissue. response in shoots, hypocotyls, and roots. The Dicot shoots generally grow in a simple radial plastids in these mutants do not sediment towards pattern. In Arabidopsis, the in¯orescence stem con- gravity in shoots, and the reduced-starch mutants sists of one epidermal layer, two to three cortical also show reduced gravitropism. The response of layers, one endodermal cell layer, and a stele con- each mutant roughly corresponds to the amount of taining vascuolar systems. Each layer arises cylin- accumulated starch granules in three organs Kiss drically from the apex to the base of the shoot. The and others 1996, 1997; Kiss 2000; Weise and Kiss ®rst three layers are arranged from outside to inside 1999). in a radial symmetrical manner; Figure 1C). The Interestingly, hypocotyls of the starchless mutants hypocotyl has almost the same tissue pattern. Both show an almost normal gravitropic response when in¯orescence stems and hypocotyls of sgr1 and sgr7 they are placed in hypergravity 5g). Moreover, the mutants have no endodermal cells and show no amyloplasts in hypocotyl endodermal cells do not gravitropic response, indicating that endodermal sediment under normal conditions 1g) but sedi- cells are essential for gravitropism in both organs ment fully under hypergravity. When wild-type Fukaki and others 1998). The sgr1 and sgr7 mutants plants are placed under hypergravity, they show an are allelic to scarecrow scr) and short-root shr), re- even more rapid gravitropic response, and the am- spectively, which were isolated as mutants lacking yloplasts sediment to a greater degree. These results root endodermal cells Fukaki and others 1998; suggested that the normal distribution and move- Scheres and others 1995).
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