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First published online April 29, 2002; 10.1105/tpc.010477 American Society of Plant Biologists The Cell Wall Hydroxyproline-Rich Glycoprotein RSH Is Essential for Normal Embryo Development in ArabidopsisDepartment of Biochemistry and Molecular Biology, University of Massachusetts, Amherst, Massachusetts 01003-4505 2 To whom correspondence should be addressed. E-mail mcannon{at}bio.umass.edu; fax 413-545-3291
Although a large number of embryo mutants have been studied, mostly at the morphological level, the critical molecular and cellular events responsible for embryogenesis are unknown. Here, we report that using an enhancer-trap embryo mutant of Arabidopsis, we identified a gene, ROOT-SHOOT-HYPOCOTYL–DEFECTIVE (RSH), that is essential for the correct positioning of the cell plate during cytokinesis in cells of the developing embryo. We traced the earliest point of influence of RSH to the first asymmetrical division of the zygote. Homozygous rsh embryos were defective morphologically, had irregular cell shape and size, and germinated to form agravitropic-defective seedlings incapable of further development. The RSH gene encodes a Hyp-rich glycoprotein–type cell wall protein. RSH localized to the cell wall throughout the embryo and to a few well-defined postembryonic sites. Although several lines of evidence from previous work suggest that the cell wall is involved in development, the protein(s) involved remained elusive.
Embryogenesis in flowering plants extends from the zygote to the desiccated seed. In Arabidopsis, the early part of embryogenesis is a period of rapid and precise symmetrical and asymmetrical cell divisions (Mansfield and Briarty, 1991  ). At the same time, cell differentiation occurs and polarity is being established, resulting in the development of a body plan with bilateral symmetry and apical-basal polarity. It is accepted generally that embryogenesis is an extremely complex process dependent on the coordination of numerous specific genetic programs as well as proper communication between cells. Many of the genes involved have essential "housekeeping" functions, whereas many more undoubtedly play critical roles in the developmental events involved in pattern formation and cell differentiation (Mayer et al., 1991). Screening of mutant banks for lethal and defective embryos has yielded large numbers of mutants (Meinke, 1994; Torres Ruiz, 1998). However, the genes identified in such screens have provided useful information relevant to plant development in general rather than to embryogenesis specifically. This is to be expected, considering that most events that occur in the embryo also occur postembryonically as the plant continues to grow and develop new organs.
Several lines of evidence suggest that the cell wall is involved in development (Berger et al., 1994
Hydroxylation of the Pro residues and glycosylation occur post-translationally in the Golgi. The amino acid motifs are presumed to be important for secondary and tertiary structure, to which Ser-(Hyp)4 contributes molecular rigidity and kinks (Ferris et al., 2001
AGPs, a family of highly glycosylated HRGPs, are involved in determining cell fate during embryogenesis in carrot cell cultures. The AGP epitope recognized by JIM8 was shown to be distributed asymmetrically in cells about to divide and to be localized exclusively to the part of the cell that would become the basal cell (Pennell et al., 1992
Proteins involved in secretion and cell wall synthesis have been shown to be required for normal embryo development in Arabidopsis (Scheres and Benfey, 1999
Cytokinesis is the part of cell division whereby the cytoplasm of one cell is cleaved into two (for recent reviews, see Staehelin and Hepler, 1996
In the embryo, as in other plant parts, the positioning of the cell plate results in either symmetrical or asymmetrical cell divisions, with consequences for differentiation and development. Although a large number of embryo mutants have been studied at the morphological level, and some at the molecular level, a unifying framework of molecular and cellular events responsible for the critical steps in embryogenesis has not been established (Torres Ruiz, 1998
Embryo Mutant Identification To discover genes with important functions in embryo development, we constructed an enhancer-trap library of Arabidopsis using an engineered transposable element (3 kb) based on the Ac/Ds system (Sundaresan et al., 1995 ). The element carries the neomycin phosphotransferase II (NPT) gene on a constitutive promoter for plant selection and the  -glucuronidase (GUS) reporter gene on a minimal promoter (40 bp) bordering one end of the transposon. GUS is expressed only when it is inserted in an appropriate orientation relative to plant regulatory sequences. Such a library is ideal for identifying lines with recessive mutations, in which the homozygous progeny display the mutant phenotype and the heterozygous progeny can be used to profile the expression of the gene in question. Embryo-defective mutants were identified by a two-step process. First, germination mutants were identified by a visual screen of transposant lines on agar plates on the understanding that a proportion would be caused by embryo defects. Second, the heterozygous progeny with germination mutations were screened after self-fertilization by microscopically visualizing embryos in seed of immature siliques (Figure 1G)
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The rsh mutant was identified as a germination-defective agravitropic mutant with severely defective root, shoot, and hypocotyl and a vitreous appearance throughout. The defective seedlings grew to a maximum length of 1 to 3 mm and were incapable of surviving for more than  3 weeks, even when transferred to fresh media (Figures 1D to 1F). A morphological examination of 3027 seed from 100 siliques of 20 self-pollinated heterozygous rsh plants at the bent-cotyledon stage of development showed that 753 seed (25%) had abnormally small embryos with no obvious organ differentiation. This mendelian inheritance pattern is consistent with a single recessive embryo mutation.
The rsh Mutant Is Cytokinesis Defective Wild-type embryos have well-defined cell shapes in relation to their positions in the embryo and have a very precise set of cell divisions leading to cell differentiation and organ formation. In rsh mutants, a zygote with a mutant phenotype was not identified; however, the position of the cell plate at the first division of the zygote differed from that in the wild type in 25% of those observed. The plane of division was in the same orientation as that of the wild type, but its position resulted in a larger apical cell relative to the basal cell compared with the wild type. In some cases, the apical cell was equal to or larger than the basal cell. The rsh mutation also affected subsequent cell divisions in the embryo, with the plane of division occurring in apparently random directions. The protoderm layer was disorganized, the hypophysis and O-ring did not develop, and abnormally shaped cells of mutant globular-stage embryos continued to divide, but bilateral symmetry was not established (Figure 2) .
The rsh Mutant Has Abnormal Cell Shapes Compared with the wild type, thin sections of rsh homozygous seedling roots showed disorganized cells with severely abnormal shapes in the epidermis, ground tissue, vascular tissue, and root cap (Figure 3) . The individual cell types differentiated to some degree, and polarity appeared to be established. Normal cell expansion did not occur, and cell growth appeared to be in random directions. The abnormal cell shapes made it impossible to determine the identity of the cell types. This is consistent with the abnormal cell shapes found in rsh homozygous embryos (Figure 2) and supports the claim that the RSH gene is essential for normal cell shape.
The RSH Gene Encodes a Putative HRGP The question of which gene (or genes) is responsible for the rsh mutant phenotype was addressed by cloning the tagged DNA contiguous to the transposon insert and using these sequences to map the insert and identify bacterial artificial chromosome clones carrying the region. A 6.5-kb EcoRI fragment of DNA was cloned from a bacterial artificial chromosome clone. Sequencing and analysis of this fragment revealed that the transposon element had inserted in chromosome I at 28 centimorgan and 228 bp upstream from the amino acid coding sequence of a putative 46.5-kD HRGP, which was on a 1.5-kb transcript with no detectable splice sites. A comparison of the plant DNA sequences at both ends of the transposon insert with that of the wild type showed that 4 bp was missing from the rsh sequence, eliminating the possibility that a large deletion at the insertion site could be responsible for the rsh phenotype (Figure 4)
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RSH has 13 nearly identical repeats of 28 amino acids each and an N-terminal transit peptide typical of cell wall–targeted proteins (von Heijne, 1985 ). The amino acid sequence of RSH has 28 Ser-(Pro)4 motifs and an abundance of Tyr, Lys, His, and Val residues, arranged mostly in repetitive motifs of Val-Lys-His-Tyr and Lys-Lys-His-Tyr-Val-Tyr-Lys, indicating that it is an extensin-type HRGP. The RSH transit peptide is identical to that of EXT3, which has 325 amino acid residues, and EXT5, which has 203 amino acid residues, both from Arabidopsis. The total amino acid sequence of RSH is related most closely to that of EXT1 (Figure 5)
. Experimentally, EXT1 was shown to be regulated developmentally. It is expressed normally in roots but not in leaves. Wounding reverses this expression pattern, causing expression in the leaves but not in roots. Salicylic acid, abscisic acid, and methyl jasmonate also elicit leaf expression of EXT1 (Merkouropoulos et al., 1999).
The rsh Mutant Phenotype Is a Consequence of a Mutation in the RSH Gene The rsh segregation and sequence data described above suggest that a mutation in the RSH gene is responsible for the mutant phenotype, and this was confirmed by two experiments. A genetic analysis of 200 seed from each of 29 heterozygous F6 generation rsh plants showed that the segregation ratio of kanamycin-resistant (selectable marker in the transposon insert) to kanamycin-sensitive plants was 2:1. None of the kanamycin-sensitive segregants to the F10 generation showed the rsh mutant phenotype. The 2:1 segregation ratio is indicative of a single embryo mutation, whereas cosegregation of the rsh phenotype with kanamycin resistance showed that the rsh mutation is not at a distant site to the kanamycin marker. It was confirmed further that expression of the RSH gene is required for normal embryo development by complementation of the mutation with the RSH transgene. Heterozygous rsh plants transformed with a 6483-bp fragment of DNA carrying the RSH gene (Figure 4) with its native regulatory sequences produced both homozygous and heterozygous rsh plants, as well as wild-type plants, carrying the T-DNA in the T1 generation. The transposants were kanamycin resistant, whereas the transformed transposants were both kanamycin and Basta resistant (see Methods). The RSH genotypes of 11 independent rsh homozygous transformants were tested by polymerase chain reaction, and the results confirmed the presence of the T-DNA in a rsh homozygous background. A wild-type phenotype with no rsh mutant segregants was observed in the T3 generation in homozygous rsh plants that were homozygous for the RSH transgene, confirming that RSH is responsible for the rsh mutant phenotype. It is worth noting that wild-type plants carrying RSH on a transgene, identified as kanamycin sensitive and Basta resistant, all had wild-type phenotypes, indicating that overproduction of RSH did not result in a mutant phenotype.
Expression Profile of the RSH Gene
Although expression was not detected before the 32-cell stage, it is likely that subdetectable levels of expression occurred, because the mutant phenotype was evident at the first division of the zygote (see below). Postembryonically, RSH was expressed at the following sites: young roots, stipules, nodes, prepollination stylar transmitting tissue, and postpollination stigma, and in wound response (Figures 6L to 6T). GUS assays of all tissue from wild-type plants were negative. Reverse transcriptase–mediated polymerase chain reaction confirmed that the GUS expression profile coincided with the tissue distribution of RSH mRNA (Figure 6U). RSH mRNA was undetected in the rsh/rsh mutant, even on extended overexposure of autoradiograms, demonstrating that the transposon insert prevented expression of the RSH gene and confirming that expression of RSH is critical for normal embryo development.
The RSH Gene Product Localizes to the Cell Wall
GUS analysis of the rsh mutant, RNA gel blot analysis, and fluorescence microscopy of wild-type plants carrying RSH::GFP all showed similar patterns of expression, supporting the claim that the GUS expression profile is an accurate reflection of RSH expression. GUS was expressed in the heterozygous and homozygous mutant embryos at equivalent stages of development, confirming that the expression of RSH in the embryo is dependent on growth stage. RSH mRNA was undetectable in the homozygous rsh mutant seedling, indicating that the enhancer trap used to generate the mutant did in fact trap the regulatory element(s) responsible for the expression of RSH and caused the rsh mutant phenotype.
The RSH gene encodes a HRGP-type cell wall protein. It is accepted generally that the HRGP family of glycosylated proteins plays a role in strengthening the cell wall; hence, these proteins most likely have functional significance in determining cell shape and plant morphology (Kieliszewski and Lamport, 1994
In carrot, the HRGP extensin-1 localizes to the cellulose layer of the cell wall (Stafstrom and Staehelin, 1988
A comparison of rsh with known embryo mutants shows that the well-studied GNOM (EMB30) mutant has the closest phenotype, in that it also has defective positioning of the cell plate at the first division of the zygote. Because GNOM encodes a protein involved in vesicular trafficking to the cell surface, it is interesting to speculate that RSH is a cargo in GNOM-associated vesicles. Subsequent to the first division of the rsh zygote, all other cell divisions produced abnormally shaped cells. This may be the consequence of the first abnormal division of the zygote or it may be attributable to the absence of RSH from cells of the developing embryo. The shape of rsh/rsh mutant cells was severely abnormal, consistent with the claim that cell shape plays a critical role in cell division (Lintilhac and Vesecky, 1984
Should RSH have a more direct function in positioning the cell plate, the following are interesting points to consider. The selection and establishment of a cortical site for cell division, and recognition of that site, are long-standing questions (Mineyuki and Gunning, 1990
In conclusion, we have profiled the expression of a gene (RSH) that encodes a HRGP-type protein, shown that its product is localized to the cell wall, and shown that its expression is critical for (1) cell shape, (2) the correct positioning of the cell plate during cytokinesis, and (3) normal embryo development. The genome sequence of Arabidopsis contains a superfamily of loosely defined putative HRGPs (Kieliszewski and Lamport, 1994
Mutant Library Construction Arabidopsis thaliana Landsberg erecta starter lines CS8047 and CS8045, carrying the engineered transposons DsE and Ac, respectively, were crossed and propagated by self-pollination to generate an F3 generation enhancer-trap library of separate F1 families, as described previously (Sundaresan et al., 1995 ).
Microscopy For fluorescence microscopy, fresh embryos removed from their seed coats at all stages of development, and fresh samples of other plant tissues, were mounted in PBS, pH 7.6. Green fluorescence was visualized using a Labophot-2 microscope (Nikon) with a fluorescence attachment and a filter set with excitation at 425 ± 60 nm and emission at 505 ± 40 nm (Chroma Technology, Brattleboro, VT). For subcellular localization of RSH, immunogold conjugated to secondary antibody and bound to anti–green fluorescent protein (GFP) antibody was viewed with a JOEL 100S transmission electron microscope at 80 kV acceleration. Heart-stage embryos and 3-day-old seedling roots of wild-type Arabidopsis transformed with pQH27 (see below) expressing RSH::GFP were examined. Seed and small pieces of root were fixed (2% glutaraldehyde, 4% paraformaldehyde, 15% picric acid, and 0.1 M phosphate buffer, pH 7.2) for 2.5 hr, washed sequentially in 0.1 M phosphate buffer, pH 7.2, three times and in water two times, each for 15 min, followed by dehydration, all at 4°C. Samples were infiltrated with resin (LR White, Medium Grade; London Resin Co. Ltd.) at 4°C for 12 to 16 hr and embedded under long-wave UV light and a stream of nitrogen gas for 12 to 16 hr at 4°C. Subsequent steps were performed at room temperature.
Sections (80 nm) were collected on formvar-coated nickel grids. Samples were blocked for 30 min with 1% BSA in PBS, pH 7.2 (PBS-1%BSA), treated with a 1:50 dilution (in PBS-0.1%BSA) of primary antibody (rabbit anti-GFP antibody; Clontech, Palo Alto, CA) for 3 hr, and washed twice, each for 2 min, in PBS containing 0.1% BSA and 0.1% Tween 20 followed by two 2-min washes in PBS-0.1%BSA. Samples were treated with a 1:20 dilution (in PBS-0.1%BSA) of secondary, goat anti-rabbit, antibodies conjugated to 10-nm gold particles (Sigma) for 1 hr in darkness and washed as described above (after exposure to primary antibodies). Samples were washed twice in water, each for 2 min, stained with 2% uranyl acetate for 10 min, washed once in water, stained with 0.5% lead citrate (Fahmy, 1967
Mapping and Cloning
GUS Localization
RNA Analyses Equal quantities of RT-PCR products were run on 2% agarose gels and stained with ethidium bromide. The 5' end of RSH mRNA was estimated by running a 5' 32P end–labeled primer extension product on a sequencing gel alongside a sequence of the same fragment. The primer extension product was obtained using the primer extension system from Promega with total RNA from wild-type plants and a primer (No. 141, 5'-CAGTTTCACTATTTTCACACTCG-3') complementary to RSH mRNA. The estimated transcription start of RSH was confirmed by the 185-bp RT-PCR fragment obtained (see above) using primers No. 129 and No. 132, because the latter is complementary to the estimated transcription start.
Transgenic Plants
The GFP fragment was inserted into the EcoRV site just downstream from the stop codon of RSH. The stop codon was eliminated subsequently by in vitro mutagenesis (QuikChange; Stratagene), leaving a RSH-GFP fusion with a 12–amino acid linker region (YISSLSIPSTSTVATM, where Y is the last amino acid of RSH and replaces the stop site, and M is the first amino acid of GFP). This 7.1-kb fragment was subcloned into the EcoRI-XhoI sites of SLJ6991, a binary-type vector carrying the kanamycin resistance marker for plant selection (Jones et al., 1992
Accession Numbers
We thank Frank Cannon (University of Massachusetts, Amherst) for useful discussions. We thank Lucy Yin and Dale Callaham at the Central Microscopy Facility of the University of Massachusetts for excellent technical assistance, and we acknowledge the National Science Foundation (Award NSF BBS 8714235) support of the facility. We also thank Jonathan Jones and colleagues at the Sainsbury Laboratory/Gatsby Charitable Foundation (Norwich, UK) for providing plasmids, and we acknowledge the ABRC at Ohio State University for providing Arabidopsis lines, BAC library arrays, and clones.
Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010477.
1 Current address: Department of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114. Received November 1, 2001; accepted January 23, 2002.
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Abstract
INTRODUCTION
