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PubMed2025

Functional genetics of rice PISTILLATA genes reveals new roles and target genes in flowering time, female fertility, and parthenocarpy.

Floral organ identity is controlled largely by the combinatorial action of MADS domain homeotic transcription factors. Lodicules are specialized plant organs in cereals and grasses that are involved in floret opening and facilitate pollination and fertility in rice (Oryza sativa L.). To understand the mechanisms underlying the specification of the rice lodicule, we investigated the developmental functions of the rice PISTILLATA (PI) paralogs, OsMADS2, and OsMADS4. Null osmads2 mutants reiterated OsMADS2 nonredundant lodicule specification roles and revealed new roles in flowering time and floral organ number and fate. Doubly perturbed osmads2 osmads4kd florets had severe abnormalities, were female infertile, yet could initiate parthenocarpy. Ubiquitous OsMADS4 overexpression rescued osmads2 abnormalities. We also utilized genome-wide binding analyses and transcriptome profiling to identify putative target genes contributing to OsMADS2 functions. In osmads2d8/d8 null mutant, we observed deregulated genes in a plethora of processes including lodicule and stamen development, floral organ number, and cell wall development. Some examples are cell division regulators (Cyclin D6, Cyclin-P4-1-like), an aquaporin (PIP1A), a peptide transporter, a vascular developmental regulator (HOX1), and a cell wall modulator (GH9B16). The deregulation of these genes may be associated with the disrupted cell division, tissue differentiation, and physiology of the malformed lodicules in osmads2 and osmads2 osmads4kd florets. Altogether, we reveal novel roles for the rice PI paralogs in flowering time, panicle exsertion, and embryo sac differentiation, identify gene targets for lodicule development, and provide mechanistic insights on the functional diversification of rice PI paralogs.

Oryza↗

PubMed2004

Conservation of B-class floral homeotic gene function between maize and Arabidopsis.

The ABC model of flower development, established through studies in eudicot model species, proposes that petal and stamen identity are under the control of B-class genes. Analysis of B- and C-class genes in the grass species rice and maize suggests that the C- and B-class functions are conserved between monocots and eudicots, with B-class genes controlling stamen and lodicule development. We have undertaken a further analysis of the maize B-class genes Silky1, the putative AP3 ortholog, and Zmm16, a putative PI ortholog, in order to compare their function with the Arabidopsis B-class genes. Our results show that maize B-class proteins interact in vitro to bind DNA as an obligate heterodimer, as do Arabidopsis B-class proteins. The maize proteins also interact with the appropriate Arabidopsis B-class partner proteins to bind DNA. Furthermore, we show that maize B-class genes are capable of rescuing the corresponding Arabidopsis B-class mutant phenotypes. This demonstrates B-class activity of the maize gene Zmm16, and provides compelling evidence that B-class gene function is conserved between monocots and eudicots.

Arabidopsis↗

PubMed2005

Functional diversification of the two C-class MADS box genes OSMADS3 and OSMADS58 in Oryza sativa.

The C-class MADS box gene AGAMOUS (AG) plays crucial roles in Arabidopsis thaliana development by regulating the organ identity of stamens and carpels, the repression of A-class genes, and floral meristem determinacy. To examine the conservation and diversification of C-class gene function in monocots, we analyzed two C-class genes in rice (Oryza sativa), OSMADS3 and OSMADS58, which may have arisen by gene duplication before divergence of rice and maize (Zea mays). A knockout line of OSMADS3, in which the gene is disrupted by T-DNA insertion, shows homeotic transformation of stamens into lodicules and ectopic development of lodicules in the second whorl near the palea where lodicules do not form in the wild type but carpels develop almost normally. By contrast, RNA-silenced lines of OSMADS58 develop astonishing flowers that reiterate a set of floral organs, including lodicules, stamens, and carpel-like organs, suggesting that determinacy of the floral meristem is severely affected. These results suggest that the two C-class genes have been partially subfunctionalized during rice evolution (i.e., the functions regulated by AG have been partially partitioned into two paralogous genes, OSMADS3 and OSMADS58, which were produced by a recent gene duplication event in plant evolution).

Amino Acid Sequence↗

PubMed2003

Pistillody is caused by alterations to the class-B MADS-box gene expression pattern in alloplasmic wheats.

Class-B floral homeotic genes are involved in specifying petal and stamen identity during flower development in plant species. Homeotic transformation of stamens into pistil-like structures (called pistillody) has been observed in alloplasmic lines of bread wheat ( Triticum aestivum L.) having the cytoplasm of a wild relative species, Aegilops crassa Boiss. To obtain information about the molecular mechanism underlying pistillody induction, we isolated two PISTILLATA ( PI)-type class-B MADS-box genes, WPI1 ( wheat PI STILLATA # 1) and WPI2, from wheat. Phylogenetic reconstruction indicated that WPI1 is orthologous to OsMADS4 and that WPI2 is probably an ortholog of OsMADS2. Both OsMADS4 and OsMADS2 genes were suggested to be PI orthologs in rice, and the function of OsMADS4 as a class-B gene was proven by the transgenic study. An in situ hybridization study demonstrated that the WPI1 gene is expressed in primordia of lodicules and stamens in developing florets in wheat. In the alloplasmic wheat line exhibiting pistillody, the WPI1 transcripts were not detected in the primordia of pistil-like stamens, whereas WPI1 was expressed in the lodicules. The wheat APETALA3 ( AP3)-type class-B MADS-box gene WAP3 ( wheat AP3) /TaMADS#82 showed an expression pattern similar to that of WPI1. These results suggest that pistillody in alloplasmic wheats is caused by alterations to the expression pattern of class-B MADS-box genes.

Amino Acid Sequence↗

PubMed2003

Functional analysis of the rice AP3 homologue OsMADS16 by RNA interference.

The rice OsMADS16 gene is phylogenetically related to the angiosperm B-function MADS-box genes. To investigate if OsMADS16 functions as an AP3/DEF orthologue to regulate the development of lodicules and stamens in rice, we isolated its genomic sequences and characterized its functions in planta by RNA interference. The genomic sequence of the OsMADS16 gene shows that it shares high similarity in genomic structure and the deduced amino acid sequence with the maize B-class gene, Si1. Transgenic lines from the introduced gene expressing double-stranded RNA with the OsMADS16 cDNA fragment were male-sterile and displayed alternations of lodicules and stamens, occasionally depressed palea and overgrown glume. The two lodicules were converted into four palea/lemma-like organs and some stamens into carpels. Further investigations of the transcription of OsMADS16 gene in these transgenic lines by RT-PCR revealed that its transcript was significantly reduced. Transcription of a rice PI homologous gene, OsMADS4, was also reduced remarkably in the transgenic plants. Our results demonstrate that OsMADS16 is an AP3/DEF orthologue to specify the identities of lodicules and stamens in rice flower and also support that OsMADS4 is a PI orthologue. In addition, these results suggest that RNA interference is a useful tool for functional genomics in rice.

Amino Acid Sequence↗

PubMed2001

Characterization of three GLOBOSA-like MADS-box genes from maize: evidence for ancient paralogy in one class of floral homeotic B-function genes of grasses.

Floral homeotic B-function genes are involved in specifying the identity of petals and stamens during flower development in higher eudicotyledonous plants. Monocotyledonous plants belonging to the grass family (Poaceae) have very similar B-function genes, except that these genes specify lodicules rather than petals. All B-function genes known so far are members of the MADS-box gene family encoding transcription factors. In some eudicot model systems such as Arabidopsis and Antirrhinum, the B-function is provided by heterodimeric protein complexes encoded by one DEF- and one GLO-like gene. In several different lineages of flowering plant species, however, more than one DEF- or GLO-like gene is found. A known example is the monocot model system rice, which contains two GLO-like genes, termed OSMADS2 and OSMADS4. Duplications of floral homeotic genes may have played a critical role in the diversification of floral homeotic functions and thus the evolution of flowers. In order to date the gene duplication event that gave rise to these two genes, we cloned cDNAs of three different GLO-like genes from maize, a distant relative of rice within the Poaceae family. Phylogeny reconstructions and chromosomal mapping indicate that one of these genes, named ZMM16, is orthologous to OSMADS2, and that the other two, ZMM18 and ZMM29, are probably orthologous to OSMADS4. The gene duplication which gave rise to OSMADS2- and OSMADS4-like genes occurred probably after the split of the lineages that resulted in extant Liliaceae and Poaceae, but before the separation of the lineages that gave rise to extant maize and rice about 50 MYA. Northern and in situ hybridization studies demonstrated that the maize genes are expressed in lodicules, stamens and carpels throughout spikelet development in male and female inflorescences. The GLO-like genes from rice have very similar patterns of mRNA accumulation. In addition, ZMM16 shows also weak expression in vegetative organs. Conservation of the expression in lodicules and stamens is in perfect agreement with a floral homeotic B-function of the GLO-like genes in grasses. The conserved expression in carpels is discussed. Moreover, circumstantial evidence for a functional diversification of GLO-like genes in grasses is provided.

Amino Acid Sequence↗

PubMed2000

Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A, B and C genes.

The floral morphology of grass species is distinct from that of typical dicot plants. In order to achieve a better understanding of the molecular basis for this diversion, we isolated RAP1A, RAP1B and RAG, putative rice orthologs for the Arabidopsis class A gene APETALA1 (AP1) and class C gene AGAMOUS (AG). The expression patterns of RAP1A, RAG and OsMADS2, a rice ortholog of the class B gene, were analyzed by in situ hybridization. RAP1A mRNA was expressed in the apical region of the floral meristem at an early stage of spikelet development, and then its expression was localized in developing lemma, palea and lodicules. The OsMADS2 transcript was first observed in the region where stamen primordia are formed. Soon after, OsMADS2 mRNA appeared in the lodicule primordia as well as the stamen primordia, and this RNA accumulation pattern persisted until late stages of floral development. The expression of RAG was observed in stamens and pistils of wild-type young spikelets. These RNA accumulation patterns are mostly similar to those of Arabidopsis class A, B, C genes, supporting the notion that the ABC model may be extended to rice.

Amino Acid Sequence↗

PubMed2003

Double-stranded RNA interference of a rice PI/GLO paralog, OsMADS2, uncovers its second-whorl-specific function in floral organ patterning.

Unlike many eudicot species, grasses have duplicated PI/GLO-like genes. Functional analysis of one of the rice PI/GLO paralogs, OsMADS2, is reported here. Our data demonstrate its essential role in lodicule development and implicate the second PI/GLO paralog, OsMADS4, to suffice for stamen specification. We provide the first evidence for differential contributions of grass PI/GLO paralogs in patterning second- and third-whorl floral organs.

Flowers↗

PubMed2007

Conservation of B class gene expression in the second whorl of a basal grass and outgroups links the origin of lodicules and petals.

Studies of flower development in core eudicot species have established a central role for B class MADS-box genes in specifying petal and stamen identities. Similarly in maize and rice, B class genes are essential for lodicule and stamen specification, suggesting homology of petals and lodicules and conservation of B class gene activity across angiosperms. However, lodicules are grass-specific organs with a morphology distinct from petals, thus their true homology to eudicot and nongrass monocot floral organs has been a topic of debate. To understand the relationship of lodicules to the sterile floral organs of nongrass monocots we have isolated and observed the expression of B class genes from a basal grass Streptochaeta that diverged before the evolution of lodicules, as well as the outgroups Joinvillea and Elegia, which have a typical monocot floral plan. Our results support a conserved role for B function genes across the angiosperms and provide additional evidence linking the evolution of lodicules and second whorl tepal/petals of monocots. The expression data and morphological analysis suggest that the function of B class genes should be broadly interpreted as required for differentiation of a distinct second floral whorl as opposed to specifying petal identity per se.

Flowers↗

PubMed2003

SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice.

We analyzed recessive mutants of two homeotic genes in rice, SUPERWOMAN1 (SPW1) and DROOPING LEAF (DL). The homeotic mutation spw1 transforms stamens and lodicules into carpels and palea-like organs, respectively. Two spw1 alleles, spw1-1 and spw1-2, show the same floral phenotype and did not affect vegetative development. We show that SPW1 is a rice APETALA3 homolog, OsMADS16. In contrast, two strong alleles of the dl locus, drooping leaf-superman1 (dl-sup1) and drooping leaf-superman2 (dl-sup2), cause the complete transformation of the gynoecium into stamens. In these strong mutants, many ectopic stamens are formed in the region where the gynoecium is produced in the wild-type flower and they are arranged in a non-whorled, alternate pattern. The intermediate allele dl-1 (T65), results in an increase in the number of stamens and stigmas, and carpels occasionally show staminoid characteristics. In the weakest mutant, dl-2, most of the flowers are normal. All four dl alleles cause midrib-less drooping leaves. The flower of the double mutant, spw1 dl-sup, produces incompletely differentiated organs indefinitely after palea-like organs are produced in the position where lodicules are formed in the wild-type flower. These incompletely differentiated organs are neither stamens nor carpels, but have partial floral identity. Based on genetic and molecular results, we postulate a model of stamen and carpel specification in rice, with DL as a novel gene controlling carpel identity and acting mutually and antagonistically to the class B gene, SPW1.

Amino Acid Sequence↗

PubMed2005

ABERRANT PANICLE ORGANIZATION 1 temporally regulates meristem identity in rice.

We report a recessive mutation of rice, aberrant panicle organization 1 (apo1), which severely affects inflorescence architecture, floral organ identity, and leaf production rate. In the wild-type inflorescence, the main-axis meristem aborts after forming 10-12 primary branch primordia. However, in apo1, the main-axis meristem was converted to a spikelet meristem after producing a small number of branch primordia. In addition, the branch meristems in apo1 became spikelet meristems earlier than in wild type. Therefore, in the inflorescence, the apo1 mutation caused the precocious conversion of the meristem identity. In the apo1 flower, lodicules were increased at the expense of stamens, and carpels were formed indeterminately by the loss of meristem determinacy. Vegetative development is also affected in the apo1. Leaves were formed rapidly throughout the vegetative phase, indicating that APO1 is also involved in temporal regulation of leaf production. These phenotypes suggest that the APO1 plays an important role in the temporal regulation of both vegetative and reproductive development.

Cell Differentiation↗

PubMed2006

The rice heterochronic gene SUPERNUMERARY BRACT regulates the transition from spikelet meristem to floral meristem.

Regulating the transition of meristem identity is a critical step in reproductive development. After the shoot apical meristem (SAM) acquires inflorescence meristem identity, it goes through a sequential transition to second- and higher-order meristems that can eventually give rise to floral organs. Despite ample information on the molecular mechanisms that control the transition from SAM to inflorescence meristems, little is known about the mechanism for inflorescence development, especially in monocots. Here, we report the identification of the SUPERNUMERARY BRACT (SNB) gene controlling the transition from spikelet meristem to floral meristem and the floral organ development. This gene encodes a putative transcription factor carrying two AP2 domains. The SNB:GFP fusion protein is localized to the nucleus. SNB is expressed in all the examined tissues, but most strongly in the newly emerging spikelet meristems. In SNB knockout plants, the transition from spikelet meristems to floral meristems is delayed, resulting in the production of multiple rudimentary glumes in an alternative phyllotaxy. The development of additional bracts interferes with subsequent floral architecture. In some spikelets, the empty glumes and lodicules are transformed into lemma/palea-like organs. Occasionally, the number of stamens and carpels is altered and an ectopic floret occurs in the axil of the rachilla. These phenotypes suggest that snb is a heterochronic mutant, affecting the phase transition of spikelet meristems, the pattern formation of floral organs and spikelet meristem determinancy.

Amino Acid Sequence↗

PubMedDate not supplied

Isolation, mapping, and characterization of two barley multiovary mutants.

Mutations in homeotic genes disturb the spatial and temporal patterns of development, often leading to the appearance of tissues in abnormal locations. Many homeotic genes, involved in flower development, code for proteins with a highly conserved domain called the MADS box, which acts as a sequence-specific DNA binding protein. Two floral development mutants were isolated from a fast neutron irradiated M2 barley population. The phenotypes are multiovary, that is, stamens replaced with carpels, designated mo7a, and stamens replaced with carpels and lodicules converted to leaflike structures, designated mo6b. These phenotypes resemble the Arabidopsis mutants APETALA3 (AP3) and PISTILATA (PI). The mo6b and mo7a mutants were mapped to the centromeric region of chromosome 1 (7H) and to the telomeric region of chromosome 3 (3H), respectively.

Alleles↗

PubMed2006

[Morphological and anatomical characterization of a stripe mutant with abnormal floral organs in rice].

A rice double mutant was derived from the transgenic process,but it does not carry the alien gene. The mutant showed white stripe on stem, leaf and spikelet. In some growing stage,the leaf started to produce fork or curliness. The floret number increased, showing multi-lemma/palea, palea-like or lemma-like lodicules or enlarged lodicules, additional pistil and stamen and the spited floret. With observation of cell ultra structure using electron microscope,the white tissue showed concaved cell wall and abnormal plastid which could not develop normal lamellae and thylakoid. The contents of chlorophyll and net photosynthesis rate in the mutant were obviously lower than those in the wild type. The cells in green sectors grow normally with the exception of the bigger cell volume. The morphogenesis of floral organ was observed by using the scanning electron microscopy (SEM). Results showed that the stamen development was not synchronal and the sizes of stamen primordium were different in mutant, and the carpel was smaller than that of wild type.

Flowers↗

PubMed1999

Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system.

A MADS family gene, OsMADS6, was isolated from a rice (Oryza sativa L.) young flower cDNA library using OsAMDS1 as a probe. With this clone, various MADS box genes that encode for protein-to-protein interaction partners of the OsMADS6 protein were isolated by the yeast two-hybrid screening method. On the basis of sequence homology, OsMADS6 and the selected partners can be classified in the APETALA1/AGAMOUS-LIKE9 (AP1/AGL9) family. One of the interaction partners, OsMADS14, was selected for further study. Both genes began expression at early stages of flower development, and their expression was extended into the later stages. In mature flowers the OsMADS6 transcript was detectable in lodicules and also weakly in sterile lemmas and carpels, whereas the OsMADS14 transcript was detectable in sterile lemmas, paleas/lemmas, stamens, and carpels. Using the yeast two-hybrid system, we demonstrated that the region containing of the 109th to 137th amino acid residues of OsMADS6 is indispensable in the interaction with OsMADS14. Site-directed mutation analysis revealed that the four periodical leucine residues within the region are essential for this interaction. Furthermore, it was shown that the 14 amino acid residues located immediately downstream of the K domain enhance the interaction, and that the two leucine residues within this region play an important role in that enhancement.

Amino Acid Sequence↗

PubMed2006

Characterization and expression of 42 MADS-box genes in wheat (Triticum aestivum L.).

MADS-box genes form a large family of transcription factors and play important roles in flower development and organ differentiation in plants. In this study, 42 wheat cDNAs encoding putative MADS-box genes were isolated. BLASTX searches and phylogenetic analysis indicated that the cDNAs represented 12 of the 14 MADS-box gene subfamilies. TaAGL14 and TaAGL15 formed a new subfamily along with a rice gene OsMADS32. RT-PCR analysis revealed that these genes had different exprsssion patterns in different organs of different stages. Expression patterns of TaAGL1 and TaAGL29 were also determined using in situ hybridization. TaAGL1 was abundantly expressed in primary root tips and the whole spikelet with more intense labeling at lodicules, paleas and stamens. TaAGL29 was expressed in both the non-reproductive parts (lemma, palea and glumes), and stamens and pistils. Moreover, differential expression patterns of these genes were also observed between wheat hybrid and its parents in leaf, stem and root of jointing stage, some were up-regulated while others were down-regulated in hybrid as compared to its parents. We concluded that multiple MADS-box genes exist in wheat genome and are expressed in tissue-specific patterns, and might play important roles in wheat growth and development.

Amino Acid Sequence↗

PubMed2003

Alteration of floral organ identity in rice through ectopic expression of OsMADS16.

We used a transgenic approach and yeast two-hybrid experiments to study the role of the rice ( Oryza sativa L.) B-function MADS-box gene, OsMADS16. Transgenic rice plants were generated that ectopically expressed OsMADS16 under the control of the maize ( Zea mays L.) ubiquitin1 promoter. Microscopic observations revealed that the innermost-whorl carpels had been replaced by stamen-like organs, which resembled the flowers of the previously described Arabidopsis thaliana (L.) Heynh. mutation superman as well as those ectopically expressing the AP3 gene. These results indicate that expression of OsMADS16 in the innermost whorl induces stamen development. Occasionally, carpels had completely disappeared. In addition, ectopic expression of OsMADS16 enhanced expression of OsMADS4, another B-function gene, causing superman phenotypes. In the yeast two-hybrid system, OsMADS16 did not form a homodimer but, rather, the protein interacted with OsMADS4. OsMADS16 also interacted with OsMADS6 and OSMADS8, both of which are homologous to SEPALLATA proteins required for the proper function of class-B and class-C genes in Arabidopsis. Based on the gene expression pattern and our yeast two-hybrid data, we discuss a quartet model of MADS-domain protein interactions in the lodicule and stamen whorls of rice florets.

Base Sequence↗

PubMed1998

Identification of class B and class C floral organ identity genes from rice plants.

The functions of two rice MADS-box genes were studied by the loss-of-function approach. The first gene, OsMADS4, shows a significant homology to members in the PISTILLATA (PI) family, which is required to specify petal and stamen identity. The second gene, OsMADS3, is highly homologous to the members in the AGAMOUS (AG) family that is essential for the normal development of the internal two whorls, the stamen and carpel, of the flower. These two rice MADS box cDNA clones were connected to the maize ubiquitin promoter in an antisense orientation and the fusion molecules were introduced to rice plants by the Agrobacterium-mediated transformation method. Transgenic plants expressing antisense OsMADS4 displayed alterations of the second and third whorls. The second-whorl lodicules, which are equivalent to the petals of dicot plants in grasses, were altered into palea/lemma-like organs, and the third whorl stamens were changed to carpel-like organs. Loss-of-function analysis of OsMADS3 showed alterations in the third and fourth whorls. In the third whorl, the filaments of the transgenic plants were changed into thick and fleshy bodies, similar to lodicules. Rather than making a carpel, the fourth whorl produced several abnormal flowers. These phenotypes are similar to those of the agamous and plena mutants in Arabidopsis and Antirrhinum, respectively. These results suggest that OsMADS4 belongs to the class B gene family and OsMADS3 belongs to the class C gene family of floral organ identity determination.

Cloning, Molecular↗