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First published online October 24, 2008; 10.1104/pp.108.128231 Plant Physiology 149:235-244 (2009) © 2009 American Society of Plant Biologists
RETARDED PALEA1 Controls Palea Development and Floral Zygomorphy in Rice1,[W]School of Life Science and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (Z.Y., S.G., L.-T.L., S.-Y.D., X.Y., D.-B.Z.); State Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou 310006, China (D.-W.X., Q.Q.); Key Laboratory of Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Graduate School of the Chinese Academy of Sciences, Shanghai 200032, China (D.L.); and Plant Sciences Division, School of Biosciences, University of Nottingham, Loughborough, Leicestershire LE12 5RD, United Kingdom (Z.A.W.)
Poaceae, one of the largest flowering plant families in angiosperms, evolved distinct inflorescence and flower morphology diverging from eudicots and other monocots. However, the mechanism underlying the specification of flower morphology in grasses remains unclear. Here we show that floral zygomorphy along the lemma-palea axis in rice (Oryza sativa) is partially or indirectly determined by the CYCLOIDEA (CYC)-like homolog RETARDED PALEA1 (REP1), which regulates palea identity and development. The REP1 gene is only expressed in palea primordium during early flower development, but during later floral stages is radially dispersed in stamens and the vascular bundles of the lemma and palea. The development of palea is significantly retarded in the rep1 mutant and its palea has five vascular bundles, which is similar to the vascular pattern of the wild-type lemma. Furthermore, ectopic expression of REP1 caused the asymmetrical overdifferentiation of the palea cells, altering their floral asymmetry. This work therefore extends the function of the TCP gene family members in defining the diversification of floral morphology in grasses and suggests that a common conserved mechanism controlling floral zygomorphy by CYC-like genes exists in both eudicots and the grasses.
Morphological innovations are critical for the diversification of animals and plants to adapt to new environments and floral bilateral symmetry is an evolutionary adaptation that facilitates out-crossing by attracting pollinators (Cubas, 2004  ). Angiosperm flowers typically grow in patterns of monosymmetry (zygomorphy, bilateral symmetry), polysymmetry (actinomorphy, radial symmetry), or left-right asymmetry with one, several, or no symmetric plane (Endress, 1999, 2001). Phylogenetic and systematic studies confirm that zygomorphic flowers have evolved several times from radially symmetric ancestors (Endress, 2001; Cubas, 2004). Investigations in Antirrhinum majus (Veronicaceae), a model plant with bilaterally symmetrical flowers, revealed that the development of zygomorphic flowers requires the activity of CYCLOIDEA (CYC) and DICHOTOMA (DICH; Luo et al., 1996, 1999; Schwarz-Sommer et al., 2003), whose function is mediated through specific interaction with the MYB genes RADIALIS and DIVARICATA (Galego and Almeida, 2002; Corley et al., 2005). The CYC and DICH genes are members of the TCP gene family, coined from the conserved basic helix-loop-helix TCP domain found in TEOSINTE BRANCHED1 (TB1) in maize (Zea mays), CYC in A. majus, and the proliferating cell factor DNA-binding proteins of rice (Oryza sativa; Cubas et al., 1999a). This family has only been identified in angiosperms and shown to be involved in specifying plant morphology. Phylogenetic analysis indicates that continuous expansion of the TCP genes from genomic duplication events may have occurred in both higher and lower plants (Navaud et al., 2007). Several studies also show that repeated and independent recruitment of CYC-like genes might be a conserved evolution pathway in controlling zygomorphic flower development within eudicots (Coen and Nugent, 1994; Cubas et al., 1999a, 1999b; Hileman et al., 2003; Cubas, 2004; Citerne et al., 2006; Feng et al., 2006; Wang et al., 2008). However, evidence of TCP genes controlling floral zygomorphy outside eudicots is lacking.
Poaceae (grasses) is one of the largest flowering plant families in angiosperms, with about 10,000 species and 700 genera, including many economically important crops such as rice, barley (Hordeum vulgare), and maize (Clayton and Renvoize, 1986
Phylogenetic analyses, along with morphological studies, indicate that zygomorphy has evolved several times in monocotyledons, and enhancing or retarding organs within specific whorls renders the monocot bilateral symmetry flower (Rudall and Bateman, 2004
Characterization of Floral Asymmetry in Rice
In this article, we propose that rice floret structure has bilateral symmetry along the Le/Pa axis, comprising lemma, palea, and lodicules in relation to their unique position and morphology (Fig. 1A
). To be consistent with previous observations, we used the developmental stages defined by Ikeda et al. (2004)
In addition to the asymmetric patterning of the rice floret, the outer whorl organs lemma and palea have distinctive cellular morphology (Prasad et al., 2005 ). Although the lemma and palea have very similar histology and both of them comprise silicified cells (sc), fibrous sclerenchyma (fs), spongy parenchymatous cells (spc), and nonsilicified cells (nsc; Fig. 2, A–C
; Supplemental Fig. S1D), the palea has distinctive marginal tissue, which is absent in the lemma (Figs. 1A and 2C). This marginal tissue of the palea (mtp) differs from the rest of palea in a unique smooth epidermis, which lacks epicuticular, silicified thickening (Fig. 2C). Another striking difference between the lemma, palea, and lodicules is that they have different vascular tissue patterns (i.e. the lemma has five vascular bundles, whereas three exist in the palea; Fig. 2A, arrows; Ikeda et al., 2004; Prasad et al., 2005). While in lodicules, several vascular trachea elements are dispersed in the parenchyma cells (Supplemental Fig. S1G, arrowheads). As a result, coupled with the asymmetric position pattern, the rice floret presents bilateral symmetry along the Le/Pa axis according to the organ identities (Fig. 1A, sky-blue arrow), which is quite different from the floral symmetry defined in the core eudicots in relation to petal adaxial/abaxial position and morphology (Cubas, 2004).
Identification and Isolation of the rep1 Mutants
To reveal the molecular mechanism regulating rice floret asymmetric development, we identified a mutant with a defect in palea morphology, rep1-1, from our rice mutant library, which is in the japonica subspecies 9522 background, created by using Compared to the wild-type growth pattern, rep1-1 showed no obvious difference during vegetative growth (Supplemental Fig. S2, A and B). At the heading and flowering stage (In 9), the morphology of the rachis, primary, and secondary inflorescence branch also displayed normal morphology in the rep1-1 mutants (Supplemental Fig. S2, C–E), and the rep1-1 spikelet showed normal development of rudimentary and empty glumes, lemma, two lodicules, six stamens, and one pistil as seen in wild-type plants from stage Sp 4 to Sp 8 (Fig. 1B). The main defect of the rep1-1 floret was only observed at the palea position commencing at stage Sp 4 with the formation of palea primordium, as shown in Figure 1B. Compared to that of the wild-type plants, the rep1-1 palea primordium seemed smaller and the developmental process was dramatically delayed (Fig. 1B). By the stage In 9, the rep1-1 palea differed significantly from wild type, appearing undifferentiated and pale (Fig. 1B). This was further supported by longitudinal sections that showed abnormal development of the rep1-1 palea during the formation of lodicule and stamen primordia (stages Sp 5 and Sp 6; Supplemental Fig. S2, G and H). Another mutant with a palea defect, designated rep1-2, was obtained as a natural variant of ZF86 (indica; Supplemental Fig. S3A) and an allelism test indicated that rep1-2 was an allele of rep1-1. These morphological studies demonstrated that the palea development of rep1-2 is significantly retarded and that the rep1-2 mutant exhibits an identical phenotype to that of rep1-1 (Fig. 2, A, B, and D; Supplemental Fig. S3), despite the different genetic backgrounds. The defect in the rep1 florets therefore appears to disrupt zygomorphic floral symmetry by suppressing palea development, although the growth pattern of both the stamens and lodicules in the rep1 mutant was not obviously affected (Figs. 1, A and B, and 2D; Supplemental Fig. S1, G and H). Genetic and molecular studies on the rep1 mutants therefore provide a valuable resource to help elucidate the molecular mechanism controlling palea development and the establishment of rice floral asymmetry along the Le/Pa axis.
To identify the REP1 gene, we used a map-based cloning approach and localized the REP1 locus between two insertion-deletion (InDel) markers on chromosome 9, CH910 and CH911, which covered bacterial artificial chromosome (BAC) AP005707, AP005683, and AP005093 (Fig. 3A ). By sequencing rep1-1 genomic DNA, we revealed that there was an approximate 42-kb deletion between the two InDel markers in the rep1-1 genome. Within this 42-kb region, there are six annotated genes in National Center for Biotechnology Information (NCBI) and The Institute for Genomic Research (TIGR; Fig. 3A), and we speculated that one of these, Os09g24480, encoding a predicted TCP domain protein, was the candidate gene related to the rep1-1 mutant. In agreement with this, a 13-bp deletion was also found in Os09g24480 of the rep1-2 genome (Fig. 3A), causing a frame shift and premature translational termination (Fig. 3, A and B, arrows). Furthermore, the Os09g24480 was confirmed to be REP1 by a functional complementation experiment using the DNA fragment carrying the wild-type genomic fragment, including a 2,968-bp promoter and a 726-bp gene sequence (REP1com; see "Materials and Methods" for detailed information), which was able to rescue the retarded palea phenotype of the rep1-1 plants (Supplemental Fig. S2F).
To further identify the coding sequences (CDS) for functional annotation of the REP1 gene, RACE-PCR was performed with the GeneRacer kit (Invitrogen) according to the user's manual. To our surprise, CDS of the REP1 gene does not match the sequence in the TIGR database in which the CDS length of LOC_Os09g24480 is predicted to be 777 bp, consisting of two exons (exon 1 runs from 1–715 bp and exon 2 from 1,518–1,579 bp of the genomic sequence). However, our RACE-PCR results show that the REP1 cDNA is 1,376 bp in length and does not contain any introns. The actual REP1 CDS runs from 1 to 729 bp with a 448-bp 5'-untranslated region (UTR) and a 199-bp 3'-UTR (Fig. 3; accession no. EU702407 [REP1]). The new 3'-terminal sequence was further confirmed using 3'-terminal specific sequences as primers for reverse transcription (RT)-PCR analysis (Fig. 4A ).
The REP1 protein was predicted to be a TCP family transcription factor in the NCBI and TIGR Web site, and our bioinformatics analysis and previous reports indicate that REP1 can be grouped into the CYC/TB1 subfamily with higher similarity to Os08g33530/OsTCP15, OsTB1, CYC, and DICH (Supplemental Fig. S4; Feng et al., 2006 ; Navaud et al., 2007; Yao et al., 2007). Therefore, functional analysis on REP1 will provide new insight toward elucidating whether there are TCP members defining the diversification of floral morphology in grasses.
As we described above, the rep1 mutations suppress palea development and disturb the establishment of the Le/Pa axis, but have minimal effect on rice vegetative growth and other flower organ development. To test the relationship between REP1 expression pattern and the rep1 phenotype, we first detected REP1 expression by RT-PCR using total RNA extracted from vegetative and reproductive organs. No REP1 transcript was detected in the vegetative organs such as root, stem, and leaf (Supplemental Fig. S5A) or in the inflorescence primordia from stage In 1 to In 4, when the inflorescence length was <0.5 cm (Fig. 4A). However, we observed the REP1 transcript at a low level in inflorescences of 0.5 to 4 cm in length when floral organs differentiate rapidly around stage In 7 (Fig. 4A). Interestingly, the REP1 transcript was detectable mainly in the stamens from the premeiosis stage to mature pollen stage (Supplemental Fig. S5B). In addition, the deletion in the rep1-2 mutant also appeared to produce a null allele of the REP1 gene because no REP1 signal could be detected in the rep1-2 inflorescence (Supplemental Fig. S5C). This could also explain why rep1-1 and rep1-2 display identical palea defects. To precisely localize the expression pattern of REP1 in rice flowers, RNA in situ hybridization was performed on sections of wild-type inflorescences containing various stages of developing florets. Consistent with RT-RCR analysis, no obvious REP1 signal could be detected when the first and secondary rachis branch primordia emerged from stage In 1 to In 4 (Fig. 4B). The earliest expression of REP1 was observed asymmetrically in the palea primordia of the apical flowers on the primary and secondary branches at stage Sp 4, no signal was seen in the lodicules and lemma positions at this stage (Fig. 4, C–E). After the initiation of stamen primordia at stage Sp 6, the REP1 signal was clearly detected in stamens, palea, and lemma, but the signal was dispersed (Fig. 4F). Around stage Sp 8 during the development of pistil and stamen, the REP1 signal appeared stronger, radially in stamens and vascular bundles of lemma and palea (Fig. 4, G and H). Only background levels of signal were observed with the REP1 sense probe (Fig. 4I). The distinctive expression pattern of REP1 of initial asymmetrical expression and subsequent radial expression may therefore be critical in controlling rice palea development and floral morphology.
To understand the role of REP1 on both palea development and the establishment of floral morphology at the cellular level in rice, the effects of REP1 on cell proliferation and differentiation during lemma and palea development were examined histologically. Compared to the cellular pattern of the wild-type floret described above, the rep1-1 lemma had no significant alternation and developed sc, fs, spc, and nsc (Supplemental Fig. S1, D and E); however, the rep1-1 palea cells seemed much smaller and less differentiated, with no clearly differentiated sc, fs, spc, and nsc (Fig. 2, A, B, D, and E). In addition, from the transverse sections we observed, five smaller vascular bundles in the rep1-1 palea (Fig. 2A, arrow), as seen in the lemma, suggesting that there may have been a partial developmental transformation from palea to lemma, occurs in the rep1-1 mutant (a similar observation was also seen in the rep1-2 mutant; see Supplemental Fig. S3B). In the rep1-1 palea, even though the cell number was observed to be very close to that of wild type at stage Sp 8 (the innermost nsc no. was about 112 ± 2.5 in wild type and 110 ± 1.6 in rep1-1; n = 6), its cell size was obviously smaller than that of wild type (Fig. 2, A and B) and during later development, around stage In 8, the rep1 palea cells still remained less differentiated (Fig. 2, D and E; Supplemental Fig. S3, C and D). This result implies that loss of function of REP1 may dramatically affect the palea cell growth and expansion, especially in the epicuticula, the innermost cell layer, and vascular tissues (Fig. 2). The alteration of palea cell morphology in the rep1 mutant was also observed by scanning electron microscopy (SEM) at stage In 8 (Fig. 2). Unlike that of wild type, the rep1-1 palea did not have the distinctive marginal tissue structure and most of the rep1-1 epicuticula grew smoothly without obvious silicified cells, imitating mtp-like cell growth patterns. Only a small part of epidermis differentiated to sc (Fig. 2C) and eventually the rep1-1 palea appeared bilaterally asymmetrical (Fig. 2, A, C, and D). These results also suggested that epicuticular thickening may be a necessary process for establishing palea identity.
To further test the cellular function of REP1, we constitutively expressed REP1 in wild-type rice under the control of the 35S promoter. In total, 63 transformants with near identical phenotypes were obtained, and one line, OEx-5 (REP1OEx line 5), was selected for phenotypic analysis; ectopic expression of REP1::GFP signal obviously can be detected in this line in the lemma and palea organs (Supplemental Fig. S6C). In the complementation test, the REP1::GFP fused construct with REP1 promoter was able to rescue the defects of rep1-1, suggesting that REP1::GFP has biological function in rice. The vegetative growth of the OEx-5 appeared normal as wild type and the lemmas, lodicules, and inner whorls of the OEx-5 also had no visible differences compared with wild type (Supplemental Fig. S6). However, the development of palea of OEx-5 seemed abnormal (Supplemental Fig. S6B) and its mtp on one side of the palea displayed sc features (Fig. 2, C and D), and the palea cell size also appeared larger than that of wild type, especially in the mtp region (Fig. 2, B and E). Therefore, this result suggests that REP1 is indeed involved in enhancing palea cell differentiation and expansion. And, based on the fact that the OEx-5 palea showed asymmetrical differentiation of the mtp (Fig. 2C), we speculate that there may be an internal (IN) symmetry regulation pathway controlling palea bilateral development. Consistent with this hypothesis, recent work on isolation of the symmetric petals1 mutant in pea indicated that IN asymmetry for pea petal development was controlled by SYP1 (Wang et al., 2008
The floral architecture in angiosperms falls into two major types, one with zygomorphic symmetry, such as in Antirrhinum, and the other with radial symmetry, as in Arabidopsis (Arabidopsis thaliana), petunia (Petunia hybrida), or tomato (Solanum lycopersicum; Coen and Nugent, 1994 ). Much progress has been made in understanding the genetic control of flower asymmetry in A. majus and other eudicots. Nevertheless, it is still of great interest to elucidate the genetic control of this developmental process in other plants, such as the grasses that have evolved unique flower and inflorescence structures.
Emerging work is beginning to shed some light on the genes that regulate the development of spikelet organs (for review, see Zanis, 2007
Plant organogenesis mainly compromises cell proliferation, expansion, and differentiation (Li et al., 2005 Because rice has the ability to self-pollinate in the exquisite flower structure enclosed by outer whorl organs, we hypothesize that the palea mtp is an essential tissue for locking the lemma and palea, and the establishment of the rice Le/Pa axis is possibly a crucial adaptation favoring seed propagation. Abnormal development and growth of lemma, palea, or lodicules would alter zygomorphic morphology of the rice spikelet. From this point of view, REP1 is partly or indirectly involved in the establishment of asymmetry through its impact on the formation of palea. However, the fact that overexpression of REP1 failed to transform lemma into palea indicates that palea was not simply derived from lemma by recruiting REP1. In other words, there are additional factors involved in the development of palea and establishment of floral asymmetry. Further experiments to identify genes interacting with REP1 will facilitate our understanding about rice floral zygomorphy.
In this article, we isolated the rice REP1 gene using a map-based cloning strategy, which encodes a putative protein belonging to a plant-specific TCP transcription factor family. These TCP family members have previously only been identified in angiosperms and have been shown to be essential in specifying plant morphology (Navaud et al., 2007
During rice floret development, the REP1 gene is asymmetrically expressed in palea primordium during early flower development, but during later floral stages is radially dispersed in stamens, the vascular bundles of lemma, and palea. This expression pattern shows significant divergence from other CYC-like genes in eudicots, which are expressed in the dorsal regions of floral meristems, where they affect petal and stamen growth and asymmetry (Luo et al., 1996 In summary, we describe rice floral zygomorphy along the Le/Pa axis in this study and, through characterization of the palea-specific regulator, REP1, provide new insights into the morphological establishment of grass flowers, and propose that this rice TCP domain gene might have evolved to regulate palea development and rice floral zygomorphy. Further molecular study on rice relatives, especially in basal grass with symmetric sepals, or asymmetric androecium, would facilitate understanding of the link between REP1-like protein expression and grass flower asymmetric structure.
Plant Materials
Plant growth conditions were as previously described (Chu et al., 2006
Inflorescences at successive developmental stages were collected from wild-type and the mutant plants over 3 to 5 d from August to September. The materials were fixed in formaldehyde-acetic acid, then sectioned and viewed with a Zeiss light microscope. SEM was performed as we described previously (Li et al., 2006
The REP1 locus was first mapped to a region closely linked to a sequence-tagged site marker E61552 on the long arm of chromosome 9 by using 10 F2 plants of rep1-1 and Guang-lu-ai 4 (spp. indica). Then, by using 738 F2 plants, the REP1 locus was narrowed to a region between two InDel markers, CH910 and CH911. Mutations in rep1-1 and rep1-2 were determined by PCR amplification and sequence analysis.
To obtain the full-length cDNA of REP1, total RNA was isolated using TRIzol reagent (Invitrogen) from wild-type inflorescence as previously described (Li et al., 2006
Gene-specific primers REP1-RTF and REP1-RTR were used for RT-PCR analysis with 38 to 40 cycles following protocol as we describe previously (Li et al., 2006
Primers REP1-CF1 and REP1-CR1 were used for complementary clone construction. The 3,694-bp genomic DNA fragment including 2,968-bp promoter and 726-bp gene sequence was ligated into pDONR201 entry vector and then pGWB4 destination vector (Invitrogen; Os09g24480pro2968bp::Os09g24480gDNA726 bp::sGFP, named REP1com in this article) for rice transformation in rep1-1 background. For ectopic expression of REP1, a 726-bp gene cDNA was amplified with primers REP1-AF and REP1-CR1, and this REP1 fragment was ligated into pDONR201 entry vector and pGWB5 vector (35S::Os09g24480gDNA726 bp::sGFP, named REP1OEx in this article) for transformation in 9522 cultivar background. For Agrobacterium-mediated rice transformation, constructs were transformed into Agrobacterium strain EHA105, and transformation of rice followed the protocol described by Nishimura (2006) Sequence data from this article can be found in the GenBank/EMBL data libraries under accession number EU702407.
The following materials are available in the online version of this article.
We thank B. Han (Rice Genome Resource Center) for providing the BAC clone. We gratefully acknowledge M.J. Cheng and Z.J. Luo for mutation screening and generating F2 populations for mapping, C.X. Ying for assistance with in situ hybridization, X.S. Gao, J.Q. Li, and Z.P. Zhang for SEM analyses, L. Zhang for assistance with the illustrations, and Ning Jiang for helpful suggestions and critical reading of the manuscript. Received August 19, 2008; accepted October 20, 2008; published October 24, 2008.
1 This work was supported by the National Basic Research Program of China (grant no. 2009CB941500), National "863" High-Tech Project (grant no. 2006AA10A102), National Natural Science Foundation of China (grant nos. 30725022, 30600031, and 90717109), and Shanghai Leading Academic Discipline Project (grant no. B205). 
2 These authors contributed equally to the article. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Da-Bing Zhang (zhangdb{at}sjtu.edu.cn).
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.108.128231 * Corresponding author; e-mail zhangdb{at}sjtu.edu.cn.
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ABSTRACT
RESULTS
-ray radiation as previously reported (Li et al., 2006
2 [3:1] = 0.064; P > 0.5), indicating monofactorial recessive inheritance of the mutant characteristic. 
