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First published online October 1, 2004; 10.1104/pp.104.050583 Plant Physiology 136:3095-3103 (2004) © 2004 American Society of Plant Biologists The gravitropism defective 2 Mutants of Arabidopsis Are Deficient in a Protein Implicated in Endocytosis in Caenorhabditis elegans1,[w]Carnegie Institution, Department of Plant Biology, Stanford, California 94305 (R.A.S., W.L., P.S., C.R.S); Department of Biological Sciences, Stanford University, Stanford, California 94305 (R.A.S., C.R.S.); and Graduate School of Biological Sciences, Nara Institute of Science and Technology, Nara 630–0101, Japan (T.K., M.T.)
The gravitropism defective 2 (grv2) mutants of Arabidopsis show reduced shoot phototropism and gravitropism. Amyloplasts in the shoot endodermal cells of grv2 do not sediment to the same degree as in wild type. The GRV2 gene encodes a 277-kD polypeptide that is 42% similar to the Caenorhabditis elegans RME-8 protein, which is required for endocytosis. We hypothesize that a defect in endocytosis may affect both the initial gravity sensing via amyloplasts sedimentation and the subsequent more general tropic growth response.
Higher plants sense their orientation with respect to the gravity vector through the sedimentation of starch-filled organelles, the amyloplasts (Sack et al., 1986  ). In stems this occurs in the endodermis (Fukaki et al., 1998), and in roots it occurs in the columella cells of the root cap. Changes in amyloplast sedimentation are thought to trigger a signal transduction cascade that mediates the relocalization of auxin transporters. Altered auxin flow causes a compensatory asymmetric growth response (for review, see Sack, 1991).
Several agravitropic mutants have been identified in which various aspects of this process are altered (Masson et al., 2002
In the sgr2, sgr3, and zig (zigzag)/sgr4 mutants, amyloplasts in the endodermal cells of the shoot do not sediment according to the gravity vector, while amyloplasts in the columella cells of the root sediment normally (Morita et al., 2002
Auxin is transported basipetally, from the shoot tips to the roots, through the polar localization of efflux carriers in the plasma membrane (Galweiler et al., 1998
We have isolated mutations in a novel gene, termed GRAVITROPISM DEFECTIVE 2 (GRV2), that result in a reduction of gravitropic responses in the hypocotyls and shoots. Based on its sequence similarity to the Caenorhabditis elegans protein RME-8 (Zhang et al., 2001
grv2 Mutations Affect Gravitropic Responses of the Shoots But Not the Roots
The grv2 mutants were identified in two independent mutant screens as plants with pronounced shoot agravitropism. In wild-type plants, primary inflorescence shoots grow upright in the opposite direction to the gravity vector. The lateral shoots also grow in a vertical direction (Fig. 1A). By contrast, grv2 primary inflorescence shoots curve slightly, and the lateral shoots grow in a horizontal direction (Fig. 1B). This growth pattern is similar to that of the sgr3, sgr5, and sgr6 mutants (Fukaki et al., 1996a
In addition, the grv2 mutant plants are slightly smaller and have reduced vigor compared to wild type. The hypocotyl elongation rates of the mutants were lower than in the corresponding wild-type strains (Table I). The final hypocotyl lengths of the mutants were also reduced relative to the wild types. In the Col alleles, a reduction in cell size accounts for the overall reduction in hypocotyl lengths. By contrast, in the Ler allele the reduced size of the hypocotyl cells was not, by itself, sufficient to account for the reduced hypocotyl length. Thus, in the grv2-1 allele, there is a defect in cell division as well. The Ler allele also has a reduction in fertility due to variable defects in stamen growth and pollen dehiscence. Manual pollination circumvents this defect and restores fertility.
To measure the gravitropic response of grv2 shoots, bolting stems of wild-type and grv2 plants were placed in a horizontal orientation. Both wild type and grv2 initially hung downward toward the gravity vector. The upward curvature of Ler (wild-type) plants reached 70 degrees within 180 min (Figs. 1C and 2A). By contrast, grv2-1 shoots showed little curvature in 180 min and even after 24 h failed to respond (Figs. 1D and 2A). Col (wild-type) shoots showed faster tropic response than Ler shoots, curving 60 degrees within 90 min. grv2-2, -3, and -4 (Col) alleles showed little gravitropic curvatures within 90 min, but they showed weak gravitropic curvature within 180 min (Fig. 2A).
Since many agravitropic mutations affect gravity responses specifically in some organs but not in others, we also examined the gravitropic responses of grv2 hypocotyls and roots. Hypocotyls of 3-d-old etiolated wild-type seedlings showed negative gravitropism and, when placed horizontally, curved upward. Etiolated hypocotyls from grv2-1 and grv2-4 showed a slight reduction in negative gravitropism (Fig. 2B), whereas grv2-2 and grv2-3 responded to the same degree as wild type (supplemental data, available at www.plantphysiol.org). The reduction in gravitropism in grv2 hypocotyls is sufficiently weak that we are not able to exclude the possibility that it is simply due to a growth defect rather than a gravitropic defect. Wild-type roots showed positive gravitropism, growing downwards toward the gravity vector. All four grv2 alleles also showed normal positive gravitropism (Figs. 2C and 3). Taken together, the gravitropic responses of grv2 mutants, reduced gravitropism of hypocotyls and shoots but normal gravitropism of roots, are similar to the phenotypes observed in sgr1, sgr2, sgr4, and sgr7.
Phototropism To test if grv2 mutations have an effect on tropic growth in general, we examined the phototropic response of grv2 shoots and hypocotyls. Wild-type Col shoots showed circumnutational motion, i.e. growth with oscillating direction. By contrast, Col alleles of grv2 caused an absence of circumnutation but a strong phototropic response (Fig. 4A). Ler wild-type stems showed no detectable circumnutation or phototropism at the light intensities used here. The Ler allele grv2-1 also did not display detectable circumnutation but did show a slight curvature toward the light. These results indicate that grv2 shoots are not deficient in phototropic responses but, to the contrary, have a tendency to respond more strongly than wild type. This can perhaps be attributed to their dampened gravitropic responses, which might not be as effectively counterbalancing phototropic stimuli as in wild type.
Etiolated wild-type hypocotyls, both from Ler and Col seedlings, curve toward the light when exposed to a lateral light source. By contrast, grv2-1 (Ler background) and grv2-4 (Col background) hypocotyls showed reduced curvature toward the light (Fig. 4B), and grv2-2 and -3 (Col) showed a slightly reduced response (supplemental data). The reduced phototropic response in hypocotyls is in sharp contrast to the enhanced phototropic phenotype in inflorescence stems. It is not clear if this is due to fundamental differences between the phototropic response in the two organs or to differences in how phototropism is assayed in each organ.
Within the organs of the shoot, gravity is sensed in a specialized layer of cells, termed endodermis. Endodermal cells contain amyloplasts, which are denser than the cytoplasm and sediment with gravity (Fig. 5A). The position of the amyloplasts within the cell is thought to provide the directional clue for sensing the gravity vector.
To test if the grv2 phenotype could be attributed to a defect in the process of gravity sensing, the position of the amyloplasts in the endodermal cells was determined. Longitudinal segments of inflorescence shoots were fixed, maintaining an upright orientation. In wild type, nearly all amyloplasts (74.6% Ler and 94.1% Col) were localized toward the basal end of endodermal cells (Table II) and accumulated at a distance from the cell wall (Fig. 5, A and C). In the grv2-1 mutant, a significant number of amyloplasts (48.7%) were localized to the top of the endodermal cells and especially accumulated at the corners of the cells appressed to the cell wall (Fig. 5, B and D). Amyloplast sedimentation was also reduced in grv2-2, -3, and -4 but to a lesser degree than grv2-1. Altogether, the localization of amyloplasts in grv2 endodermal cells is abnormal, as it is in the agravitropic mutants sgr2, sgr3, and zig/sgr4 (Kato et al., 2002 ; Morita et al., 2002; Yano et al., 2003). It seems possible that in all these mutants agravitropism might result from a defect in gravity sensing.
In the root, gravity is sensed through the sedimentation of amyloplasts in the columella cells. We found no difference between wild type and grv2 in the position of root amyloplasts (data not shown). This result is consistent with the observation that grv2 roots respond to gravity to the same degree as wild type.
The GRV2 gene was cloned based on its map position. The grv2 mutation is closely linked to erecta, enabling selection of recombination events in the vicinity of grv2 based on the visible phenotype conferred by erecta. Using PCR-based markers, grv2 was mapped to an approximately 70-kb interval in the bacterial artificial chromosome clones F12C20 and T20P8. A contig of binary T-DNA cosmids spanning this region (Fig. 6A) was established and the cosmids transformed into grv2 mutant plants. A single cosmid, pRAM011, containing three genes (At2g26870, At2g26880, and At2g26890) complemented the grv2 phenotype. One of the three genes, a MADS box gene (At2g26880), was completely contained on two other cosmids, pRAM051 and pRAM052, which did not complement grv2. The grv2-1 and grv2-4 alleles of the remaining two genes were sequenced. No mutations were found in At2g26870, a putative phospholipase. However, mutations in At2g26890 were found in both alleles (see below). A 15.3-kb genomic fragment spanning from 2 kb upstream to 1 kb downstream of the predicted At2g26890 coding sequence complemented the grv2 mutant phenotype. We conclude that GRV2 corresponds to At2g26890.
To determine the intron/exon structure of GRV2, we analyzed the sequence of a partial cDNA clone (RZL04ho7) and nine reverse transcription-PCR products (Fig. 6B). Our results confirmed the predicted intron/exon structure. GRV2 transcripts are 11.8 kb long with a 7,665-bp coding region predicted to encode a 277-kD protein. The GRV2 gene contains 21 introns (Fig. 6B).
Domain searches revealed that the GRV2 gene product contains a single Dna-J domain (amino acid position 1,500–1,588) and four IWN repeats (Fig. 6B; supplemental material). GRV2 shows 26% identity and 42% similarity over the entire protein with the C. elegans gene product RME-8 (Zhang et al., 2001
The grv2-1 allele, which was induced by ethyl methane sulfonate, has a G-to-A transition resulting in a stop codon 85 amino acids from the native stop codon. In the grv2-4 allele, which was induced by gamma rays, 13 bp in exon 10 (ATGCGAGCAGAAA) are substituted by a stretch of 14 unrelated bp (CTATCACTTTCAAT). The resulting frame shift creates a stop codon in exon 11. Two T-DNA insertions in the coding region of GRV2 were identified in the Cold Spring Harbor Laboratory (Sundaresan et al., 1995
RNAse protection assays indicated that GRV2 is expressed at similar levels in roots, rosette leaves, stems, cauline leaves, flowers, and siliques (Fig. 7). This result is corroborated by publicly available data from whole-genome microarrays (supplemental data). Plants expressing the reporter gene
Gravitropic responses can be broken down into three consecutive steps: perception of the gravity vector in specialized cells, transduction of the resulting signal to the surrounding tissue, and coordinated asymmetric growth of the organ. Perception of the gravity vector is mediated by the sedimentation of amyloplasts that results in mechanical pressure on cellular components such as the endoplasmic reticulum, cytoskeleton, or internal membranes. This mechanical stimulus is thought to trigger an unknown signal transduction cascade and, ultimately, to regulate auxin flux. Mutants lacking starch have more buoyant plastids with different sedimentation properties and show slower and less pronounced gravitropic responses than wild type (Caspar and Pickard, 1989 ).
The inflorescence shoots of grv2 mutants exhibit three abnormalities related to tropisms: reduced response to gravity, extended horizontal growth of lateral shoots, and enhanced response to light. A related syndrome of abnormalities was also observed in the sgr mutants (Fukaki et al., 1996b
These reduced gravitropic responses might also indirectly cause the enhanced phototropic responses of shoots of grv2 mutants. Gravitropism is thought to be one of the factors responsible for circumnutational movements, the other being most likely an internal oscillator (Hatakeda et al., 2003 Hypocotyls of grv2 mutants also exhibit a slight defect in the gravitropic response, as well as, in contrast to shoots, a reduction in the phototropic response. Given the reduction in the growth rates of grv2 hypocotyls, it is possible that these tropic defects may actually be due to general growth defects rather than specific gravity or light response defects.
Cloning of GRV2 revealed that it is similar to CeRME-8, which encodes a protein required for endocytosis in C. elegans. The first allele of CeRME-8 was isolated in a screen for temperature-sensitive mutations. At the permissive temperature, this allele causes a reduction in receptor-mediated endocytosis of yolk protein into oocytes. At the restrictive temperature, fluid-phase endocytosis from the body cavity, the pseudocoelom, into scavenger cells, coelomocytes, is also impaired. CeRME-8 localizes to the periphery of large vesicles that appear to be endosomes, but its specific biochemical function is not known (Zhang et al., 2001
A complete block in endocytosis in a eukaryotic cell is expected to be lethal because it would prevent recycling of membrane components required for maintaining vesicle-mediated secretory processes. Indeed, the temperature-sensitive rme-8 mutant is lethal at the restrictive temperature indicating that RME-8 is essential in worms. Likewise, all 17 alleles of DmRme-8 are also embryonic lethal (Chang et al., 2004
There are no structurally similar genes to GRV2 in the Arabidopsis genome that could compensate for the loss of GRV2 function. Thus, since it seems unlikely that a plant can survive with a complete loss of endocytosis, grv2 mutations likely could result either in generally inefficient endocytosis and membrane recycling or in the loss of a specific membrane transport pathway. Both scenarios could perceivably have a dramatic impact on the endomembrane system. Preliminary results using the dye FM1-43 as a general marker for endocytosis do not show any dramatic differences between grv2-1 and the wild type (data not shown). The sgr2, sgr3, and zig/sgr4 mutations are thought to primarily affect the tonoplast membrane, causing alterations in vacuole morphology and dynamics (Morita et al., 2002
An alternative hypothesis is that a defect in grv2 prevents proper cycling of proteins from the plasma membrane to the internal membrane network. This could, for example, affect the normal turnover of auxin efflux carriers via endocytosis and polarized secretion (Geldner et al., 2001
Based on our current data, it is not possible to distinguish between the two models. It is conceivable that a defect in endocytosis could affect gravitropism in both the sensing step and the asymmetric growth response. This may be the case for zig/sgr4, which has a defect in amyloplasts sedimentation and a 35% decrease in auxin transport in hypocotyls, though it does not dramatically change the localization of PIN1 or PIN3 (Surpin et al., 2003
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The grv2-1 mutant was isolated from an ethyl methane sulfonate-mutagenized population in the Ler ecotype. The grv2-2 (renamed from sgr8-1), grv2-3 (sgr8-2), and grv2-4 (sgr8-3) alleles were isolated in the Col ecotype. The grv2-2 and grv2-3 alleles were isolated from a fast neutron-mutagenized population, and the grv2-4 allele was isolated from a gamma ray-mutagenized population. Additional T-DNA insertions in GRV2 were obtained from publicly available collections at the Cold Spring Harbor Laboratory (GT1669; Sundaresan et al., 1995 To determine the growth rates, seedlings were grown on the surface of agar medium in vertically oriented petri plates containing Murashige and Skoog medium with 1.5% Suc and 0.8% agar in the dark at 23°C. Hypocotyl lengths were measured every 12 h for 7 d. Cell lengths were measured in the fully elongated hypocotyls on day 7.
Intact stems of 4-week-old plants, 4 to 8 cm tall, were placed horizontally in the dark at 23°C. In 90-min intervals from 0 to 180 min, the curvature of the stem was measured as the angle between the basal region of a primary inflorescence shoot and the growing tip. To assay the hypocotyl and root gravitropic response, seedlings were grown on Murashige and Skoog medium as described above. Three days after germination, the orientation of the seedlings with respect to gravity was changed to horizontal. The curvature of both hypocotyls and roots were measured at various times thereafter as described previously (Fukaki et al., 1996a
White light (25–35 µmol m–2 s–1) was applied from the side of the inflorescence shoots in 4-week-old plants (4–8 cm). The degree of curvature of stems was measured every 30 min for 3 h. To assay the hypocotyl phototropic response, seedlings were grown on Murashige and Skoog medium as described above. Three-day-old etiolated seedlings growing vertically were illuminated with horizontal white light 10 to 40 µmol m–2 s–1 for 24 h, and the curvature of the hypocotyls was measured at intervals as described previously (Fukaki et al., 1996a
Stem segments (2–3 cm below the apex) cut from primary inflorescence stems were fixed in 4% paraformaldehyde in phosphate buffer, pH 6.8, overnight at 4°C. The growth orientation of the stem was maintained during fixation. Stem segments were dehydrated through an ethanol series and embedded in Technovit 7100 (Heraeus Kulzer, Wehrheim, Germany) according to the manufacturer's instructions. Sections (4 µm) were stained for 5 min with 0.5% toluidine blue. Amyloplasts were viewed with a compound microscope by 400x magnification and counted at the top and bottom of cells.
Stem segments (2–3 cm below the apex) cut from primary inflorescence stems were fixed in 4% formaldehyde, 2% glutaraldehyde in 0.01 M sodium phosphate buffer, pH 6.8, overnight at 4°C. The growth orientation of the stem was maintained during fixation. Samples were postfixed in 1% osmium tetroxide for 1.5 h, dehydrated in an ethanol series, and embedded in Spurr's resin. Silver-gold sections (60–90 nm) were stained with 2% uranyl acetate (7 min), lead citrate (1 min), and viewed with a JEOL 1230 transmission electron microscope, manufactured in Japan.
The grv2-1 mutant was crossed to Col wild-type plants to generate an F2 mapping population. Analysis with PCR-based markers indicated that grv2 mapped approximately 2 cM south of erecta. Using the visible phenotype of erecta mutants, recombinants in the grv2-1 erecta interval were selected for fine mapping. Polymorphisms between Col and Ler were identified by sequencing and from the Cereon collection (Jander et al., 2002
A cosmid library made from the Col ecotype in the binary cosmid vector pBIC20 (Meyer et al., 1994
Total RNA was isolated from Landsberg wild-type plants using Trizol reagent (Invitrogen, Carlsbad, CA). cDNAs were synthesized from flower RNA using Moloney murine leukemia virus reverse transcriptase (Promega, Madison, WI) and primers specific for GRV2, 5'-CACGGCTGAGGACCTTG-3' and 5'-CCACAACACAACCTTCG-3'. Nine cDNA fragments were amplified from the primary transcripts by PCR using the following primer pairs: 5'-GGGAGGCCTTAGTAAGAATAAGC-3' and 5'-GCATTTGCACCGGAGAGACACCG-3'; 5'-CATCGGGACGTGTATGC-3' and 5'-ATCTGCGGACTCTGCTGGGTTTGTTCTGT-3'; 5'-TCGACATCACCAGGGGAA-3' and 5'-GTTGAGAGACGAATAG-3'; 5'-CCCTCCACCAAAACCATCAAGCCTACTCA-3' and 5'-CAGTGATGGATGTCCAGTTC-3'; and 5'-CATCCATTCCTTAGGTGGTTCC-3' and 5'-CCACACGGAGAGACTACCC-3'. The PCR products, as well as a truncated expressed sequence tag, were sequenced to determine the intron/exon structure of the GRV2 transcripts.
Radioactively labeled GRV2 and UBC1 (Sullivan and Viersta, 1991 The sequence of GRV2 is deposited with the EMBL/GenBank data libraries under accession number NM_128246.
We thank Rob Martienssen, Joe Ecker, and colleagues for providing indexed T-DNA insertion lines, Kazusa DNA Research Institute for providing expressed sequence tag clones, and P. Poindexter for technical assistance. We thank D. Bergmann and W. Briggs for comments on the manuscript. Received May 26, 2004; returned for revision July 27, 2004; accepted July 27, 2004.
1 This work was supported in part by grants from the U.S. Department of Energy (grant no. DOE–FG02–00ER20133), the U.S. Department of Agriculture Cooperative State Research, Education, and Extension Service (grant no. CSREES 00–35304–9394), the National Institutes of Health Cellular and Molecular Biology Training Program (grant no. 2–T32–GM007276 to R.A.S.), and the Human Frontiers Science Project organization (grant no. LT–594–96 to W.L.). 
2 These authors contributed equally to the paper.
3 Present address: Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724.
4 Present address: Division of Biology 159–29, California Institute of Technology, 1200 East California Boulevard, Pasadena, CA 91125.
[w] The online version of this article contains Web-only data. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.050583. * Corresponding author; e-mail crs{at}stanford.edu; fax 650–325–6857.
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niewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415: 806–809
