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First published online July 9, 2004; 10.1104/pp.104.041996 Plant Physiology 135:1502-1513 (2004) © 2004 American Society of Plant Biologists Overexpression of OsRAA1 Causes Pleiotropic Phenotypes in Transgenic Rice Plants, including Altered Leaf, Flower, and Root Development and Root Response to Gravity1Research Center for Molecular and Developmental Biology, Key Laboratory of Photosynthesis and Environmental Molecular Physiology, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China
There are very few root genes that have been described in rice as a monocotyledonous model plant so far. Here, the OsRAA1 (Oryza sativa Root Architecture Associated 1) gene has been characterized molecularly. OsRAA1 encodes a 12.0-kD protein that has 58% homology to the AtFPF1 (Flowering Promoting Factor 1) in Arabidopsis, which has not been reported as modulating root development yet. Data of in situ hybridization and OsRAA1::GUS transgenic plant showed that OsRAA1 expressed specifically in the apical meristem, the elongation zone of root tip, steles of the branch zone, and the young lateral root. Constitutive expression of OsRAA1 under the control of maize (Zea mays) ubiquitin promoter resulted in phenotypes of reduced growth of primary root, increased number of adventitious roots and helix primary root, and delayed gravitropic response of roots in seedlings of rice (Oryza sativa), which are similar to the phenotypes of the wild-type plant treated with auxin. With overexpression of OsRAA1, initiation and growth of adventitious root were more sensitive to treatment of auxin than those of the control plants, while their responses to 9-hydroxyfluorene-9-carboxylic acid in both transgenic line and wild type showed similar results. OsRAA1 constitutive expression also caused longer leaves and sterile florets at the last stage of plant development. Analysis of northern blot and GUS activity staining of OsRAA1::GUS transgenic plants demonstrated that the OsRAA1 expression was induced by auxin. At the same time, overexpression of OsRAA1 also caused endogenous indole-3-acetic acid to increase. These data suggested that OsRAA1 as a new gene functions in the development of rice root systems, which are mediated by auxin. A positive feedback regulation mechanism of OsRAA1 to indole-3-acetic acid metabolism may be involved in rice root development in nature.
The growth and development of crops depend on their roots to take up water and nutrient material from soil. The root system of rice (Oryza sativa) consists of embryonic and postembryonic roots. The rice embryonic roots, originating from the radical, emerge after germination. They develop into two forms, one primary root and several seminal roots. Postembryonic roots include adventitious roots that are formed from nodes of the plant and lateral roots that develop on all root types.
As is known, plant hormone auxin (indole-3-acetic acid [IAA]) plays an important role in controlling root development, such as inhibiting elongation of a primary root and promoting formation of adventitious roots, lateral roots, and root hairs. In Arabidopsis, it has been reported that genes involved in the auxin signal transduction pathway are able to control the development of roots. For example, mutants of the AUX/IAA gene family, such as SHY2/IAA3, SLR1/IAA14, IAA28, and MSG2/IAA19, show reduced lateral roots or no lateral roots (for review, see Reed, 2001
Auxin is possibly synthesized in young leaves and root meristem (Thimann, 1977
In Arabidopsis, many genes, such as the AUX/IAA family, the SAUR (small auxin up-regulated RNA) family, and the GH3 family (Hagen et al., 1984
In monocot plants, the molecular mechanism that establishes the morphology of root systems is blurry so far. Only a small number of mutants related to root formation were found in monocots. For example, rtcs mutant is completely devoid of all adventitious roots (Hetz et al., 1996 In this paper, we used a reverse genetics approach to study the functions of a novel auxin-induced gene regulating root development in rice. Based on the database of expression sequence tag (EST) and genomic sequences, a cDNA and its promoter sequence were cloned. Its expression patterns and phenotypes of overexpression in transgenic plants were analyzed.
OsRAA1 Gene Encodes a Small Protein and Is Conserved in Plants Based on the EST database, an unknown small protein gene corresponding to an EST (AU071162) was identified in rice (BAB07982. A PAC clone (P0462H08) containing the EST was screened from the database of DDBJ/GenBank/EMBL. The RACE strategy was utilized to amplify the full-length cDNA in rice. The full-length cDNA consists of 725 nucleotides containing a 327-nucleotide open reading frame (ORF). The 5'-upstream untranslated region is 82-bp long, and the 3'-downstream untranslated region is 339-bp long. The ORF was predicted to encode a 109-amino acid polypeptide with a calculated molecular mass of 12 kD and a pI of 9.45 (Fig. 1A). There are three amino acids that are slightly rich in protein: Ser, Val, and Leu. It was named OsRAA1 (Oryza sativa Root Architecture Associated 1) since our data suggested that its functions are related to root morphology development in rice. Comparative analysis between sequences of the cDNA and those of the PAC clone (P0462H08) at chromosome 1 in rice suggested that the OsRAA1 gene has no intron.
The results of BLAST in the GenBank showed that OsRAA1 shared a 58% sequence homology of amino acids with AtFPF1 (Flowering Promoting Factor 1; Y11988). A series of ESTs, including MossFPF1 (AW699964) from moss (Physcomitrella patens); ChrFPF1 (BE034410) and ChrFPF2 (BE033961) from chrysanthemum root; MuFPF1 (Y11987) from mustard; ZeTaP1 (BE552830) from the cDNA library of maize tassel primordia; WhRoP1 (BE428690) and WhRoP2 (BE428819) from the wheat root library; and BaLeP1 (BE421936), BaSpP1 (BG342901), and BaSpP2 (BE196402) from the barley leaf library and spike library, were also obtained from the database (Fig. 1, B and D). The analysis showed that homologous genes of OsRAA1 exist ubiquitously from the lower plant (such as moss) to the higher plant (such as chrysanthemum). It indicates that this gene family may play important roles in plant development. Comparative alignments analysis of the OsRAA1 sequence suggested that four conserved domains presented in these proteins. The first motif is -GVWV/IF- in the N-terminal part; the second one is -GWERYY- in the middle part; and the third and fourth ones are -DLIS/ALP- and -H/YMYDI/VVV/I- in the near C-terminal part, respectively (Fig. 1C). Interestingly, the conservative domains except for the second one appear in the hydrophobic region on the hydrophobicity plot (data not shown). Besides that, there were seven Leu conserved. There are at least three members of this gene family in Arabidopsis (Y11988, T04505, and T49976). In rice, there is another EST (AU070455) shared sequence with OsRAA1. The complete sequence corresponding to the EST was obtained from the GenBank (contig AAAA01001788.1). At rice chromosome 7 (AP003982), there is a fragment of genomic sequence, which can also be deduced to a protein with high homology with OsRAA1 (Fig. 1C). These three sequences in rice belong to three different subfamilies (data not shown). Phylogenetic analysis of the AtFPF1/OsRAA1 gene family indicated that homologs were divided into three branches. It also showed there are different members expressed even in the same organ (Fig. 1D). For example, there are two ESTs (WhRoP1 and WhRoP2) from the wheat root library, and they are located at different branches of the phylogenetic tree. Another two ESTs (BaSpP1 and BaSpP2) are in the barley spike library, which belong to a different subfamily. OsRAA1 is located in a branch that was different from those of AtFPF1. The OsRAA1 promoter sequence of 1,987 bp was isolated and analyzed. Elements of GA and auxin response were involved in the promoter region. The conservative GA response complex consists of pyrimidine box (C/TCTTTTC/T), GA response element (TAACAAA), and element of TATCCA. Those elements appeared in the promoter region (Fig. 1E), but it was a very weak response to GA3 treatment (data not shown). There is an auxin response element (AuRE) core sequence 5'-TGTCTC-3' located at –150 to –145 (Fig. 1E). In reverse orientation, another AuRE (5'-CTCTGT-3') is located at –158 to –153. The presence of two AuRE motifs suggested that the OsRAA1 gene is probably regulated by auxin.
The expression pattern of OsRAA1 was investigated as to its localization. Northern analysis showed that the OsRAA1 mRNA was specifically transcripted in the organs of roots and spikes (Fig. 2A). No signal was detected in either young shoots or leaves. Data of RNA in situ hybridization showed a more distinct expression pattern. As shown in Figure 2, F and G, signals of OsRAA1 were detected in the root apex, including quiescent center and dividing cells. Stronger signals were shown in the cortex of root apical meristem and pericycle of root apex. On the contrary, no distinct signal could be detected in the cortex of the mature zone. A transcript of OsRAA1 was also present in lateral roots, especially in the lateral root primordia and the pericycles of the branch zones (Fig. 2, B and C). In situ hybridization also showed that OsRAA1 mRNA is expressed in the apical meristem of young spikes (Fig. 2E). Besides that, there is a distinct signal in the collenchyma cells of margin vascular bundles between shoot and roots (Fig. 2D). As is known, the adventitious roots are differentiated from these collenchyma cells (Fujii, 1959
To further confirm the expression patterns, an expression vector of GUS (  -glucuronidase) driven by OsRAA1 promoter was constructed and transformed into rice plants. The transgenic plants showed the patterns of GUS staining in the roots, which are similar to the data of in situ hybridization described above. Figure 3A showed that strong signals were detected in lateral roots and their primordia. It was clear that there were staining signals of GUS activity in the division and elongation zones of the root apex, while there was no signal detected in root cap (Fig. 3B). GUS activity appeared in the palea/lower palea vascular strands (Fig. 3C). The conjugated part between anther and filament also showed a strong signal in the GUS transgenic plant driven by the OsRAA1 promoter (Fig. 3E). Although a few signals appeared at some parts of young leaves, they were irregular and unstable (Fig. 3D).
Therefore, mRNA of OsRAA1 is present in the rapidly growing zones, which indicates its possible roles in the cell growth and/or division. Interestingly, its expression pattern in the root was similar to that of AUX1 (Marchant et al., 2002  ) and TIR1 and NAC1 in Arabidopsis (Gray et al., 1999; Xie et al., 2000), which are involved in auxin transport or signal transduction pathway.
There were 20 independent Ubi::OsRAA1 transgenic lines with characters of a tolerance to hygromycin and a positive staining of GUS marker to be obtained from the different transformed rice callus in the experiments. Longer flag leaves of the transgenic plants were a clear phenotype in comparison with the wild-type control without a hygromycin treatment. To investigate its role in root development, the seeds of 12 independent transgenic lines with the longest flag leaves were harvested. More than 50 seeds of these lines were germinated in the half-strength MS medium with 75 mg L–1 hygromycin, respectively. Leaves of these seedlings were cut and stained with 5-bromo-4-chloro-3-indolyl-
Constitutive Expression of OsRAA1 Results in Longer Leaves and Filaments When the transgenic plants of Ubi::OsRAA1 grew for 2 weeks after germinating from a solution of hygromycin (75 mg L–1), they were transferred into the soil and then cultured in a greenhouse. The OsRAA1 gene expressed constitutively in leaf and root in the transgenic plants. During the first month after transfer, the transgenic plants grew more slowly than the wild-type controls without a hygromycin treatment. But just before the booting stage, the leaves of the transgenic plant were longer than those of the wild-type control. Especially at the heading stage, the flag leaves of the transgenic plants were distinguished as longer than those of the control plants. As shown in Table II and Figure 5A, the flag leaves of the transgenic plants were about 44 cm (up to 60 cm in some independent lines) in length on the average, while those of the wild-type controls were about 31 cm. The leaf length of transgenic plants was 1.4 times longer than the control. The results of a scan electronic microscope showed that silica cell length of the transgenic plant was longer than that of the control, which was supported by statistical tests (P < 0.05; Fig. 5D). There were five silica cells in the limited area in the flag leaf of the transgenic plants on the average, while six cells appeared at the same size area in the wild-type control (Fig. 5, B and C). In other words, the cell length of transgenic plants was 1.2 times larger than the wild-type control based on the scan electronic microscope data. The difference between the wild-type control and the transgenic plant reached a significant level in statistics (P < 0.05; Table II). It was suggested that the length increase of flag leaves in the transgenic plant might be caused by both extension of cells and an increase in cell numbers. Extension of cells, however, contributed more than increase of cell numbers to leaf extension in transgenic plants.
Abnormal florets appeared in the spikes of the transgenic plant (Fig. 5, F and G). The yellow and plump anthers of the wild-type control plant were just above penniform carpels at that stage (Fig. 5E). Conversely, stamens of the transgenic plants with OsRAA1 constitutive expression resulted in abnormally longer filaments with white and shrunken anthers (Fig. 5, F and G). Actually, some filaments were too long to be peeled off from the palea; they curved and attached tightly to the palea.
Based on the AuRE sequence in OsRAA1 promoter, the expression patterns in roots, and the phenotypes of transgenic plants with constitutive expression of OsRAA1, we hypothesize that expression of OsRAA1 gene is regulated by auxin. Northern blot showed that the OsRAA1 mRNA was increased from treatment of 10–5 M IAA. More than double expression was induced by the treatment of 10–4 M IAA (Fig. 6A). The GUS staining data of the OsRAA1::GUS transgenic plant showed that auxin induced a stronger signal in the transgenic plant, while a weaker blue signal appeared in the untreated control (Fig. 6B). Suppression of the inhibitor of auxin polar transport on GUS staining clearly occurred as the treatment time went on (Fig. 6B). The inhibitor experiment may support an explanation that decrease of endogenous auxin weakened GUS expression-driven OsRAA1 promoter. The results suggested that expression of the OsRAA1 gene in nature is induced by auxin.
The effect of auxin on root development was observed (Fig. 6). Interesting phenotypes occurred in the wild-type roots treated with 1-napthaleneacetic acid (NAA). Growth of the roots was strongly inhibited by auxin as compared with untreated wild-type control (Fig. 6, C and D; Table III). The numbers of adventitious roots, however, increased up to 11 in a treated seedling plant. In the untreated control, there were five adventitious roots under the same conditions (Table III). All of the treated plants had helix-like primary roots (Fig. 6D). The phenotypes were similar to those status in tomato that auxin stimulated lateral root growth at a concentration at which primary root growth was inhibited (Muday and Haworth, 1994 ).
In the Ubi::OsRAA1 transgenic plant, results of auxin treatment showed that a promotion role on the adventitious root initiation induced by IAA was more distinguished than that in the wild-type control (Fig. 7A). However, the adventitious root initiation responses to 9-hydroxyfluorene-9-carboxylic acid (HFCA), a polar auxin transport inhibitor, between the transgenic plants and the wild-type control exhibited similar phenotype (Fig. 7B). Results of auxin level determined showed that IAA level either in shoot or root was obviously higher in the transgenic plant of Ubi::OsRAA1 than that in the wild- type control (Fig. 8). And IAA of the transgenic shoot was 2.8 times greater than the wild-type control, while those of the root were 1.9 times greater. It suggested overexpression of OsRAA1 resulted in accumulating a higher level of IAA in the transgenic plant.
It is well known that gravitropism is a phenomenon mainly regulated by auxin. The seedlings were reoriented horizontally in the darkness to check their gravitropic response. Until reoriented for 3 h, any gravitropic response of the overexpression line was not detected, while the wild-type control showed a distinct response (Fig. 9, A, B, and D). In fact, the transgenic lines with extreme overexpression completely lost gravitropic response until reoriented for 20 h. The kinetics of gravitropic curvature showed a vigorous graviresponse from 3 h after gravistimulation in the transgenic plant (Fig. 9D). Results in Figure 9, C and D, showed that treatment of IAA obviously deferred gravitropic response in the wild-type control, which was similar to that in maize and Arabidopsis (Ishikawa and Evans, 1993 ; Yamamoto and Yamamoto, 1998; Kim et al., 2000; Ottenschlager et al., 2003). The response phenotype of the overexpression line was identical to those of treatment of IAA in the wild type. These results suggest that the constitutive expression of OsRAA1 might disturb the auxin distribution and reduce gravitropic response in rice roots.
The OsRAA1 gene belongs to a novel gene family that appears to be conserved in plants from lower to higher. Members of this gene family in both Arabidopsis and rice have no introns in their genomic sequences (Fig. 1; Kania et al., 1997 ). These characters are similar to those of the SAUR gene family. SAUR family genes have no introns and form gene clusters in their genomic sequence. Most of them encode about 10 kD, a small protein. Their expression can be regulated by auxin (McClure and Guilfoyle, 1989). The OsRAA1, however, has no obvious homology to the members of the SAUR family. So the OsRAA1 may belong to a new small protein family, which can also be regulated by auxin.
FPF1 protein was firstly studied as a flowering promoting factor in mustard (Melzer et al., 1990
The expression pattern shows that OsRAA1 transcript was always in rapidly growing cells, such as primordia of the lateral roots, the steles of young adventitious roots and lateral roots, the meristem, and the division zone of the root apex (Figs. 2 and 3). Cells of these tissues generally undergo rapid division and elongation, and auxin plays important roles in these processes (Boerjan et al., 1995
OsRAA1 gene expressed mainly in root and spike (Fig. 2). The putative auxin influx carrier AUX1 modifies root architecture to promote lateral root formation (Marchant et al., 2002
Our data in northern blot (Fig. 6A) and OsRAA1 promoter-GUS transgenic plants (Fig. 6B) suggested that the expression of OsRAA1 can be induced by auxin. The OsRAA1 gene expressed constitutively with higher efficiency in the transgenic plants (Fig. 4). Auxin regulates initiation and growth of root in diverse plants (Muday and Haworth, 1994
Constitutive expression of OsRAA1 could also delay the gravitropic response of roots. Some extreme transgenic plants showed no response at all. In Arabidopsis, gravitropic curvature of IAA-treated roots was close to zero, despite a slight but significant downward curvature. Roots on 2,4-D showed no or even tenuous upward curvature (Ottenschlager et al., 2003 OsRAA1 shows tissue-specific expression in roots and spikes, and it was induced by auxin. Constitutive overexpression of the gene resulted in the increased number of adventitious roots and reduced growth of primary roots. At the same time, other phenotypes controlled by auxin, such as root helix and gravitropic response, appeared in the roots of the transgenic plants. Overexpression of OsRAA1 increased adventitious root initiation and reduced gravitropic response in rice, which was similar to the responses of the wild-type plants to auxin. At the same time, overexpression of OsRAA1 also caused endogenous IAA to increase. Our data supported that OsRAA1 as a new gene functions in the development of rice root systems, which are mediated by auxin. A positive feedback regulation mechanism of OsRAA1 to IAA metabolism may be involved in rice root development in nature. The biochemical mechanism of the protein functioning in regulation of root development will be addressed by an approach of yeast two-hybridization and immunology.
Isolation of OsRAA1 and Construction of Vectors Total RNA of rice (Oryza sativa L. cv Zhonghua 10) root was isolated using the QIAGEN RNeasy plant mini kit (Qiagen, Valencia, CA). The mRNA was purified from total RNA using an Oligotex Poly(A) mRNA purification kit (Qiagen). Then two fragments of OsRAA1 cDNA were amplified by 5' and 3' RACE using a Marathon cDNA amplification kit (Clontech, Palo Alto, CA). The double-strand cDNA was synthesized and ligated to the Marathon cDNA adaptor. The 5'- and 3'-end cDNA sequences were amplified using Adaptor primer 1 (5'-CCATCCTAATACGACTCACTATAGGGC-3') and the ORF forward and reverse primers (5'-AGGGGTTTGGGTGTTGAAG-3' and 5'-CTAGCTCTGATTGCAAGAAGAATGAAG-3'), respectively. The whole ORF was cloned into pBluescript II SK+ (Stratagene, La Jolla, CA) and sequenced.
The cassette of UbiPro+OsRAA1+Noster was ligated into the multicloning sites of the binary vector pCAMBIA1301 to construct a vector of Ubi::OsRAA1, which carried a gene of GUS as a marker (Cambia, Canberra, Australia; Roberts et al., 1997
In situ hybridization was performed as described by Schwarzacher and Heslop-Harrison (2000)
Rice embryonic calli were induced on scutella from germinated seeds and transformed with strain EHA105 of Agrobacterium tumefaciens containing the desired binary vector, as described by Hiei et al. (1994)
Total RNA electrophoresis and the programs of the RNA transferred and cross-linked onto a nylon membrane (Hybrid N+; Amersham, Buckinghamshire, UK) were performed as described by Sambrook et al. (1989)
GUS staining was performed according to the method described by Jefferson (1989)
Treatment of IAA for Analysis of Northern Blot
Treatment of OsRAA1::GUS Transgenic Plant with NAA for Histochemical Display of GUS Activity
When the rice plants accomplished heading, the flag leaves of the Ubi::OsRAA1 transgenic plants and the untransformed control were harvested. Small blade fragments from the absolute middle part of the flag leaves were immediately fixed in FAA (3.7% formaldehyde, 50% ethanol, 5% acetic acid) for 12 h and dehydrated in a graded ethanol series. The dehydrated materials were critical point dried in liquid CO2 and mounted on metallic stubs. The mounted material shadowed with gold before viewing with the S-800 scanning electron microscope (Hitachi, Haramachi, Fukushima, Japan).
IAA level in seedling was determined by a method of ELISA, (Li and Zhou, 1996
All chemicals in the experiments were from Beijing Chemicals, Beijing except for those labeled otherwise above. Sequence data from this article have been deposited with the EMBL/GenBank data libraries under accession number AY659938.
We thank Dr. Z.Y. Wang and Dr. J.X. He (the Carnegie Institution of Washington and Stanford) and Dr. R.J. Chen (Institute of the Nobel Foundation) for their critical reading and comments on the manuscript. We thank Mrs. Wei-Min Teng for the plasmid of KSP9. and Dr. H.W. Xue (Shanghai Institute of Plant Physiology, CAS) for his help on establishment of gene transformation of rice. Received March 5, 2004; returned for revision April 6, 2004; accepted April 7, 2004.
1 This work was supported by the Major State Basic Research Program of China (grant no. G19990116), by the Innovation Grand of CAS, National Nature Science Foundation of China (NSFC; grant no. 30270143), and by the State Project of Transgenic Plant (J99–A–024) as well as the State High-Tech Project (2001AA222281).  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.041996. * Corresponding author; e-mail chongk{at}ibcas.ac.cn; fax 86–10–8259–4821.
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