the phylogeny and expression pattern of apetala2 like genes in rice

Document Sample
the phylogeny and expression pattern of apetala2 like genes in rice Powered By Docstoc
					Journal of Genetics and Genomics (Formerly Acta Genetica Sinica) October 2007, 34(10): 930-938

Research Article

The Phylogeny and Expression Pattern of APETALA2-like Genes in Rice
Meifang Tang1, Guisheng Li2, ①, Mingsheng Chen2
1. College of Animal Science and Technology, Northwest A &F University, Yangling 712100, China; 2. State Key Laboratory of Plant Genomics and Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China

Abstract: The multigene families undergo birth-and-death evolution and thus contribute to biological innovations. The APETALA2-like genes belong to the euAP2 group of the AP2 gene family. These genes are characterized by several distinct motifs and exist in ferns, gymnosperms, and angiosperms. The phylogenetic analysis indicated that these genes have undergone the birth-and-death evolution. The five APETALA2-like genes in rice (Oryza sativa L.) display redundant but distinct expression patterns as demonstrated by RT-PCR and in situ hybridization. The potential functions of these genes were discussed on the basis of phylogenetic and expression pattern. Keywords: evolutionary innovations; duplication; microRNA172

The APETALA2-like genes belong to a large family that is defined by the AP2-domain [1]. An AP2-domain is composed of approximately 68 amino acids that form a three-stranded β-sheet and an α-helix; and the APETALA2-like protein can constitute a homodimer to contact DNA via arginine and tryptophan residue in the β-sheet [2−4]. This type of protein has two tandem AP2-domains that are linked by a conservative region [1]. Additionally, the APETALA2-like genes possess one microRNA172 (miRNA172)-binding site [5]. The APETALA2-like proteins may also share one nuclear localization signal [6] and two unknown motifs [5]. The APETALA2-like genes are possibly horizontally transferred from bacteria or viruses into plants, evolving independently to other AP2-domain-containing genes [7]. In earlier studies [5, 8], the euAP2 group in ArabiReceived: 2007-04-23; Accepted: 2007-05-26

dopsis was suggested to comprise six APETALA2-like genes: APETALA2 (AP2, At4g36920), which functions in floral organ specification, stem cell maintenance, and seed mass determination
[2, 8−13]


OF EAT1 (TOE1, At2g28550), TOE2 (At5g60120), TOE3 (At5g67180), SCHLAFMUTZE (SMZ, At3g54990), and SCHNARCHZAPFEN (SNZ, At2g39250), which are involved in timing flowering [14, 15]. In rice (Oryza sativa L.) genome, there are five APETALA2-like genes in the euAP2 group [16]. The SUPERNUMERARY BRACT (SNB) may control the transition from spikelet meristem to floral meristem [6]. In Petunia hybrida L., PhAP2A is not essential to the perianth development although it can restore the ap2-1 mutant in Arabidopsis; PhAP2B and PhAP2C may play a complementary role, but are all expressed in endosperm[17]. In Antirrhinum majus L.,

This work was supported by the National Natural Science Foundation of China (No. 30600034 and 30621001) and Chinese Academy of Sciences (No. CXTD-S2005-2). ① Corresponding author. E-mail:; Tel: +86-10-6487 3487; Fax: +86-10-6487 3428

Meifang Tang et al.: The Phylogeny and Expression Pattern of APETALA2-like Genes in Rice


LIPLESS1 (LIP1) and LIP2 are required for the perianth development; however, they are not involved in the repression of the C-function genes within the perianth [18]. In Amborella, the putative sister to all other angiosperms, an APETALA2-like gene is expressed in all floral organs and leaves [5]. In gymnosperms, PtAP2L1, PtAP2L2, PaAP2L1, and PaAP2L3 are expressed in seed-bearing ovuliferous scale, while PaAP2L2 can promote the petal identity in ap2-1 mutant in Arabidopsis [19, 20]. The APETALA2like genes also exist in ferns [5]. Therefore, the phylogenetic relationship and functional divergence among APETALA2-like genes currently appear confusing. Multigene families generally undergo birth-anddeath evolution, in which genes may duplicate and members may be subject to loss, subfunctionalization, or neofunctionalization, finally possibly causing biological innovations [21]. As more and more APETALA2like genes are isolated and their functions are characterized, it will be possible to investigate how they functionally evolve to contribute to biodiversity. In this article, we exhaustively identify APETALA2-like genes and report their sequence character and phylogenetic relationship, and perform expression analysis of all five APETALA2-like genes in rice. We prove that the APETALA2-like genes undergo the birth-and-death evolution, and discuss its relationship to certain biology in rice.

the on-line database for Chlamydomanas reinhardtii D. (; and the APETALA2-like transcripts were searched using tBLASTn against the on-line database within the NCBI. Each APETALA2-like gene in rice and Arabidopsis was used as the query sequence. The AP2-domain alignments were carried out using CLUSTALX1.81[22], and were adjusted using the GENEDOC software ( genedoc). The neighbor joining tree was constructed using the MEGA3 software [23], and the maximum likelihood tree was constructed using the on-line PHYML program ( 1.3 RNA extraction and RT-PCR analysis

The total RNA was isolated with Trizol (Invitrogen, Carlsbad, California, USA) and then digested with RNase-free DNaseⅠ. First-strand cDNA was synthesized with 2 μg RNA, 10 ng oligo(dT)15 primer, and M-MLV reverse transcriptase (Promega, Madison, Wiscoson, USA). The RT-PCR was programmed: 96℃ for 3 min as the first step, 94℃ for 30 s, 52℃ for 30 s, and 72℃ for 1 min, for 28 cycles, as the second step, and then 72℃ for 10 min as the third step. PCR products were separated in a 1.2% agarose gel. PCR products were cloned into pGEM-T easy vector (Promega, Madison, Wiscoson, USA) and were sequenced in three clones. Gene-specific regions with mutual similarity no more than 68% were used to produce probes. The primer sequences used to clone APETALA2-like gene in rice were: for 07g13170, 5′ CTACCTGAAACCGACAATGAAGTGG-3′and 5′ CGTAGAGAATCCTGATGATGCTGC-3′for 03g60; 430, 5′ -CCAGACGCCGGAAATGAGGCA-3′ 5′ and GGCGCCGGCAGAGAATCCT-3′for 06g43220, 5′ ; GGCTCCTTCAGATACCAACC-3′and 5′ -GAACCCAAAGACCCTCCC-3′for 04g55560, 5′ ; -GGCCGCCGCAACCGCTACAG-3′and 5′ -GGCCATGGTGAAAGAAAAGAAGG-3′ for 05g03040, 5′ ; ACTGCCCAACCTCATCCCCTATTC-3′and 5′ -


Materials and Methods

The rice (O. sativa ssp. japonica cv. Nipponbare) calli, one-week seedlings with roots and leaves, root-tips and young leaves from one-month plants, mature leaves, and panicles at various stages were used. 1.2 Sequence collection and phylogenetic analysis The APETALA2-like proteins were searched using the HMMER program ( against the downloaded datasets from the NCBI (, and BLASTp against


Journal of Genetics and Genomics


Vol. 34 No. 10 2007

CCCGCCGGCGCAAAGACG-3′ The actin gene . was amplified by 5′ -GAGGCGCAGTCCAAGAGGGGTAT-3′and 5′ -TCGGCCGTTGTGGTGAATGAGTAA-3′ RT-PCR analysis was performed twice . and the results were identical. 1.4 RNA in situ hybridization

bated with 10 μg/mL proteinase E (Sigma, St. Louis, Missouri, USA) for 45 min at 37℃; 4) the linearized templates were used for probe preparation.


Phylogenetic analysis

The RNA in situ hybridization was performed according to Li et al. [24], with the following modifications: 1) 50% formamide was added when washing with 2 × SSC, 1× SSC, 0.5 × SSC; 2) 65℃ was used when washing with 0.5 × SSC; 3) slides were incuAPETALA2
motif 1 ATG motif 2 AP2 domain

The APETALA2-like genes were found with similar structural organizations: motif 1, motif 2, the nuclear localizing signal, the first AP2-domain, the second AP2-domain, motif 3, and the miRNA172-binding site (Fig. 1). The neighbor joining tree was constructed
AP2 domain motif 3

miRNA172 site TGA

nuclear localizing signal

TOE1_Arabidopsis thaliana SMZ_Arabidopsis thaliana SNZ_Arabidopsis thaliana TOE2_Arabidopsis thaliana PHAP2B_Petunia hybrida ABE87891_Medicago truncatula 05g03040_Oryza sativa AAZ95247_Dendrobium crumenatum IDS1_Zea mays Q_Triticum turgidum 03g60430_Oryza sativa SNB_Oryza sativa 0019003502_Populus trichocarpa AAK14326_Pisum sativum GLOSSY15_Zea mays 06g43220_Oryza sativa PHAP2A_Petunia hybrida APETALA2_Arabidopsis thaliana LIPLESS2_Antirrhinum majus LIPLESS1_Antirrhinum majus 04g55560_Oryza sativa TOE3_Arabidopsis thaliana PaAP2L1_Picea abies




Fig. 1

The structure of APETALA2 in Arabidopsis, and the sequences of motif 1 (the first sequence column), motif 2 (the

second sequence column), and motif 3 (the third sequence column) in representative APETALA2-like proteins
– represents the gap produced in the multiple alignment.

Meifang Tang et al.: The Phylogeny and Expression Pattern of APETALA2-like Genes in Rice


to infer the orthology and paralogy among 94 APETALA2-like genes from angiosperms, gymnosperms, and ferns (Fig. 2). Ten homologous genes from mosses and green algae were included as the outgroup. The maximum likelihood tree had similar topology in terms of the major clades (data not shown). Clades A and B were detected within the highly supported APETALA2-like group (bootstrap 100). Clade A (bootstrap 100) only consisted of one gene in rice, one gene in Sorghum bicolor L., and two in maize (Zea mays L.). Clade B (bootstrap 74) was very large and contained other genes including the remaining APETALA2-like genes from rice, sorghum, and maize. Clade B was further divided into two subclades, B1 and B2, although both were weakly supported (bootstrap value < 50). Each subclade included genes from angiosperms and gymnosperms. In a few species including rice and Arabidopsis, several APETALA2-like genes were identified. For example, four APETALA2-like genes were detected in Antirrhinum, and three in Populus. The APETALA2-like genes from one species sometimes were clustered together, and sometimes they individually were grouped with genes from other species. For example, five APETALA2-like genes were observed in wheat (Triticum aestivum L.), among which four formed a cluster close to 05g03040 in rice, while the Q gene was close to 03g60430 and SNB in rice (Fig. 2). 2.2 Expression pattern analysis

The temporal and spatial distribution of mRNA indicates gene function. RT-PCR was conducted to determine whether genes were transcribed in major structures including roots, leaves, and inflorescences, and in situ hybridization was performed to observe the expression pattern of genes at serial stages of panicles. Gene-specific primers were designed from exons to overcome genomic DNA contamination in the RT-PCR analysis.

BI426798 Glycine max BM892891 Glycine max BI893552 Glycine max BG447926 Medicago truncatula CV004845 Persea americana 2501 Poplus trichocarpa CO077851 Gossypium raimondii CX288343 Citrus clementina CA783794 Glycine soja CV098349 Vitis shuttleworthii ABE87891 Medicago truncatula 05g03040 Oryza sativa CA134360 Saccharum officinarum BE516333 Triticum aestivum 69 BE430033 Triticum aestivum 73 CAE53889 Triticum aestivum DW220086 Aedes aegypti 61 CJ706407 Triticum aestivum EL444408 Helianthus tuberosus CV095008 Vitis shuttleworthii EL438914 Helianthus tuberosus DY276868 Citrus clementina AAD22495 Hyacinthus orientalis BAE48514 Ginkgo biloba BAE48512 Cycas revoluta BAD36744 Ipomoea nil AJ568173 Antirrhinum majus PHAP2B Petunia hybrida 128415 Populus trichocarpa 65 BU762655 Glycine max CF452606 Allium cepa TOE1 Arabidopsis thaliana PaAP2L2 Picea abies 99 DR163776 Pinus taeda DY367730 Zingiber officinale AAZ95247 Dendrobium crumenatum DV130883 Euphorbia esula CV006845 Amborella trichopoda 54 AAY17062 Ceratopteris thalictroides 54 PaAP2L3 Picea abies BAE48516 Gnetum parvifolium PtAP2L2 Pinus thunbergii 74 Q Triticum turgidum 03g60430 Oryza sativa 73 IDS1 Zea mays SNB Oryza sativa 99 SMZ Arabidopsis thaliana 100 60 DY025037 Brassica napus SNZ Arabidopsis thaliana TOE2 Arabidopsis thaliana DV486051 Brachypodium distachy 97 DY810353 Taraxacum officinale DT768867 Aquilegia formosa DR929205 Aquilegia formosa DR933842 Aquilegia formosa DT601137 Saruma henryi 81 EL469046 Helianthus tuberosus BQ996151 Lactuca serriola BU000526 Lactuca serriola PtAP2L1 Pinus thunbergii 93 PaAP2L1 Picea abies APETALA2 Arabidopsis thaliana TOE3 Arabidopsis thaliana 80 BM412846 Solanum lycopersicum BI933811 Solanum lycopersicum BQ120583 Solanum tuberosum 100 PHAP2A Petunia hybrida 99 CG297894 Zea mays 96 62 CW353359 sorghum bicolor EE292661 Zea mays 04g55560 Oryza sativa DY331085 Ocimum basilicum LIPLESS2 Antirrhinum majus AAL57045 Malus domestica AJ568171 Antirrhinum majus LIPLESS1 Antirrhinum majus BE659939 Glycine max CX541535 Medicago truncatula AAK14326 Pisum sativum 0019003502 Populus trichocarpa DY269701 Citrus clementina DN817888 Gossypium hirsutum EB117796 Malus domestica DT556960 Gossypium hirsutum EG665779 Ricinus communis DV120287 Euphorbia esula DV633347 Cucumis melo BU047453 Prunus persica BQ401537 Gossypium arboreum 71 06g43220 Oryza sativa GLOSSY15 Zea mays 100 CG299203 Zea mays 96 96 CW160279 Sorghum bicolor 08g04050 Ostreococcus tauri 61 EE078047 Vitis vinifera 99 CD475882 Nuphar advena 100 EE613071 Helianthus argophyllus BJ178045 Physcomitrella patens 85 121738 Chlamydomonas reinhardtii 54 14g02450 Ostreococcus tauri 03g02200 Ostreococcus tauri 170879 Chlamydomonas reinhardtii 13g02090 Ostreococcus taur
60 55


Clade B2

Clade B1

Clade A


Fig. 2 The neighbor joining tree of 94 APETALA2-like genes from ferns, gymnosperms, and angiosperms, and 10 homologous genes from mosses and green algae (outgroup)
The bootstrap value below 50 was hidden. Genes from green algae were highlighted by the symbol ♦, mosses by ●, ferns by ▲, gymnosperms by ■, and rice and Arabidopsis by ▼. The accession number or gene name is shown followed by the species name.


Journal of Genetics and Genomics


Vol. 34 No. 10 2007

03g60430: The RT-PCR analysis showed that this gene is weakly expressed in panicles, mature leaves, and calli, while it is strongly expressed in roots and leaves from one-month plants (Fig. 3). A smaller transcript was observed in one-week seedlings, indicating that this gene should not be expressed, or that another alternative splicing transcript was detected.

Fig. 3 RT-PCR analysis of the APETALA2-like gene in rice
The result for the actin gene was not shown for a concise presentation. Lane 1 in each gel showed the PCR product of 07g13170 in the mature spikelet, 1-week seedling, juvenile leaf, root tip, callus, and mature leaf, etc.

When environmental conditions and internal factors become favorable for floral induction, a shoot apical meristem (SAM) that has regularly formed leaves and tillers is converted into an inflorescence meristem. The inflorescence meristem forms bracts and branches. The in situ hybridization revealed that this gene was expressed in early inflorescence meristem including emerging bract primordium, and was also expressed in the surrounding leaves (Fig. 4A). The primary branch primordium forms at the axils of bract primordium. At this stage, this gene was mainly transcribed in the primary branch primordium and

weakly in the bract primordium and leaf, but not in the rachis (Fig. 4B). Interestingly, it was localized in the corpus while not in the tunica of the primary branch primordium (Fig. 4C). The secondary branch forms at the basal region of the primary branch, which frequently produces the tertiary branch. Then, the branch meristem is converted into a spikelet primordium. The hybridization signal was observed in the whole branch meristem (Fig. 4D), which was very strong in certain area where the rudimentary glume may develop (Fig. 4E). The spikelet meristem firstly differentiates a pair of rudimentary glume and then a second pair of empty glume, and subsequently the floral meristem. At this time, the signal was observed in the spikelet meristem, two pairs of glume were stained, and the strongest signal was detected in the floral primordium (Fig. 4, G, H). Each floral meristem produces one floret consisting of one lemma, one palea, two lodicules, six stamens, and one carpel. This gene was expressed in the stamen and carpel but not in the lemma/palea and lodicule (Fig. 4, I, J). Finally, the formation of thecae and ovules encloses the floral meristem, which was reddish owing to the presence of its transcripts (Fig. 4F). 05g03040: This gene was expressed in several tissues and organs excluding mature leaves by RT-PCR analysis (Fig. 3). The results of the in situ hybridization suggested that it was expressed in the primary branch primordium (Fig. 5A) and the whole spikelet meristem before the rudimentary glume primordium emerges (Fig. 5B); it was also expressed in two pairs of glumes, differentiating floral meristem with nascent lemma/palea (Fig. 5C), the stamen and carpel (Fig. 5D), the ovule and theca (Fig. 5F). 06g43220: RT-PCR analysis suggested that this gene was expressed in one-week seedlings, young leaves and young roots from one-month plants, and was weakly expressed in mature leaves and calli, and was almost not expressed in panicles (Fig. 3). It was expressed in leaves, inflorescences with the bract primordia (Fig. 5G), ovules, and thecae (Fig. 5H).

Meifang Tang et al.: The Phylogeny and Expression Pattern of APETALA2-like Genes in Rice


Fig. 4

RNA in situ localization of 03g60430

A: the gene is expressed in differentiated shoot apical meristem with emerging bract primordium, and subtending leaf; B: signal is strong in the primary branch primordium but weak in the bract primordium. It is transcribed in the corpus but not in the tunica (C); D: the transcripts are localized where the spikelet primordium forms, and the rudimentary glume primordium shows very strong signals (E); F: the transcripts in thecae and ovules; G, H: the gene was detected in young leaves, the spikelet meristems including the rudimentary glume and empty glume, and floral primordium; I: weak signal on stamens; J: few transcripts detected on stamens and carpels; K: the control showing the bract primordium. Scale bar = 200 µm.

Fig. 5 RNA in situ localization of 05g03040 (A-F), 06g43220 (G, H), and 04g55560 (I, J)
Gene 05g03040 was expressed in the primary branch primordium (A), spikelet primordium (B), young leaf, and differentiated primary branch including two pairs of glumes, differentiating floral meristem with the lemma and palea (C), stamens and carpels (D), and thecae and ovules (F); 06g43220 was transcribed in young leaves, and the inflorescent meristem with the bract primordium (G), and in the theca and ovule (H); 04g55560 was detected in thecae and ovules (I). (E) The control showing spikelet primordia (J) .The control showing mature floret. Scale bar = 200 µm.


Journal of Genetics and Genomics


Vol. 34 No. 10 2007

04g55560: This gene was expressed in panicles, seedlings, and root-tips. And its transcripts are of low amount in young leaves, calli, and mature leaves (Fig. 3). It was also expressed in ovules and thecae (Fig. 5I). 07g13170: RT-PCR analysis revealed that this gene was expressed in panicles, one-week seedlings, young leaves, young roots at relatively high level, and in calli at low level. No transcripts were observed in mature leaves (Fig. 3). Other studies revealed that this gene is expressed in leaves, SAMs, branch meristems, spikelet meristems, and glume primordial [6]. In summary, genes 03g60430, 05g03040, 06g43220, 04g55560, and 07g13170 were all transcribed in juvenile and mature leaf, root tip, callus, theca, and ovule. Additionally, 03g60430 was expressed in the bract primordium, primary branch primordium, spikelet primordium, two pairs of the glume primordium, stamen, and carpel. Genes 07g13170 and 05g03040 were similarly expressed as 03g60430 but with significant differences. Gene 06g43220 was only expressed in the bract primordium. However, 04g55560 was not expressed in these tissues.



The APETALA2-like genes display similar sequence characters, such as the miRNA172 site, and exist in land plants including ferns, gymnosperms, and basal angiosperms. These motifs may be essential to gene function, and thus possibly play a role in evolution via the amino acid mutation. In green alga, similar genes only possess the tandem AP2-domain, and are different from the AINTEGUMENTA (ANT)-like genes which are sister to the APETALA2-like genes. Our phylogenetic tree reveals that both APETALA2- and ANT-like genes possibly exist in green alga. Then, whether the APETALA2-like gene exists in mosses is critical to understand the origin of APETALA2-like genes.

Generally, several APETALA2-like genes exist in one species, and they are clustered together or grouped with genes from other species. This pattern suggests that the APETALA2-like gene evolves under the birth-and-death model. The birth-and-death model predicts that genes are produced by duplication and some duplicates are deleted from genomes, and thus a pattern of inter-species gene clustering and the presence of the pseudogene are the hallmarks this evolutionary mode [21]. However, once the pseudogene emerges, it may accelerate to accumulate mutations, resulting in an extremely divergent sequence after a long evolutionary history; making it impossible to prove its existence on the basis of sequence similarity. This may account for the lack of APETALA2-like pseudogenes in our research. Since the birth-anddeath evolution can result in innovation [25], it is interesting to explore all five APETALA2-like genes in rice in terms of gene function which may be inferred from gene expression pattern. Gene 03g60430 is expressed in leaves, roots, inflorescences, primary branch meristems, glumes, floral meristems, stamens, carpels, ovules, and thecae. Its duplicate, SNB, displays very similar expression pattern. In the snb mutant, the transition from spikelet meristem to floral meristem is delayed, resulting in the production of multiple rudimentary glumes[6]. Their putative ortholog in wheat, Q gene, is transcribed in roots, leaves, and spikes, conferring domesticated traits such as free-threshing character, and affecting the glume shape and tenacity, rachis fragility, spike length, plant height, and spike emergence time[4]. The putative ortholog in maize, INDETERMINATE SPIKELET1 (IDS1), is expressed in roots, leaves, SAMs, inflorescence primordia, spikelet pair primordia, embryos, but not in glumes and lemmas/paleas, floral meristems, lodicules, anthers, or the gynoecium of the ear. In ids1 mutant, the spikelet meristem becomes indeterminate and produces additional florets[8]. Since these genes are putative orthologs but are differentially expressed and related

Meifang Tang et al.: The Phylogeny and Expression Pattern of APETALA2-like Genes in Rice


to morphology variation, this cluster may contribute to the evolution of raceme in grasses, as the LEAFY HULL STERILE1 (LSH1) gene[27]. Gene 06g43220 was expressed in leaves, roots, bract primordia, ovules, and thecae. Its putative ortholog in maize, GLOSSY15, is expressed in juvenile leaves[28], and plays a primary role in the maintenance of the juvenile phase[29]. This cluster had only genes from grasses (Fig. 1). Gene 04g55560 was expressed in leaves, roots, ovules, and thecae. However, its putative ortholog in Arabidopsis, AP2, is expressed in all four types of floral organs besides ovules, inflorescence meristems, leaves, and stems [2]. Another putative ortholog of this gene in Arabidopsis, TOE3, may be expressed in the inflorescence meristem, acting as a flowering repressor [14]. Gene 05g03040 was expressed in leaves, roots, spikelet meristems, floral meristems, ovules, and thecae; its potential ortholog TOE1 in Arabidopsis may only be expressed in inflorescence meristem as a flowering repressor [14, 15]. However, the expression pattern indicates that 05g03040 may be functional equivalent of AP2, reflecting the weakness in the phylogenetic tree. Thus, gene 05g03040 is possibly important to understand the genetic basis for homologous but distinctive sepal and petal in Arabidopsis and the lemma/palea and lodicule in rice [30, 31], and gene 04g55560 for the flowering time which is crucial to the plant adaptation [32]. In conclusion, the APETALA2-like gene exhibits a complex structure, and undergoes the birth-and-death evolution. Such genes may be involved in some unique biology in rice. Acknowledgments: We thank Yufeng Wu, Yi Sui, Fei Lu of Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China, for their assistance in this research. References
1 Okamuro JK, Caster B, Villarroel R, van Montagu M, Jofuku KD. The AP2 domain of APETALA2 defines a large new

family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA, 1997, 94(13): 7076−7081.[DOI] 2 Jofuku KD, Boer B, Montagu MV, Okamuro JK. Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell, 1994, 6(9): 1211−1225.[DOI] 3 Allen MD, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M. A novel mode of DNA recognition by a β-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J, 1998, 17(18): 5484−5496.[DOI] 4 Simons KJ, Fellers JP, Trick HN, Zhang Z, Tai YS, Gill BS, Faris JD. Molecular characterization of the major wheat domestication gene Q. Genetics, 2006, 172(1): 547−555.[DOI] 5 Kim S, Soltis PS, Wall K, Soltis DE. Phylogeny and domain evolution in the APETALA2-like gene family. Mol Biol Evol, 2006, 23(14): 107−120.[DOI] 6 Lee DY, Lee J, Moon S, Park SY, An G. The rice heterochronic gene SUPERNUMERARY BRACT regulates the transition from spikelet meristem to floral meristem. Plant J 2007, 49(1): 64−78.[DOI] 7 Magnani E, Sjolander K, Hake S. From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. Plant CellI, 2004, 16(9): 2265−2277.[DOI] 8 Nole-Wilson S, Tranby TL, Krizek BA. AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states. Plant Mol Biol, 2005, 57(55): 613−628.[DOI] 9 Krizek BA, Prost V, Macias A. AINTEGUMENTA promotes petal identity and acts as a negative regulator of AGAMOUS. Plant Cell, 2000, 12(8): 1357−1366.[DOI] 10 Jack T. Molecular and genetic mechanisms of floral control. Plant Cell, 2004, 16(sup. 1): S1−17. 11 Jofuku KD, Omidyar PK, Gee Z, Okamuro JK. Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc Natl Acad Sci USA, 2005, 102(8): 3117−3122.[DOI] 12 Ohto MA, Fischer RL, Goldberg RB, Nakamura K, Harada JJ. Control of seed mass by APETALA2. Proc Natl Acad Sci USA, 2005, 102(8): 3123−3128.[DOI] 13 Wurschum T, Gross-Hardt R, Laux T. APETALA2 regulates the stem cell niche in the Arabidopsis shoot meristem. Plant Cell, 2006, 18(2): 295−307.[DOI] 14 Aukerman MJ, Sakai H. Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell, 2003, 15(11): 2730−2741.[DOI] 15 Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU. Dissection of floral induction path-


Journal of Genetics and Genomics


Vol. 34 No. 10 2007

ways using global expression analysis. Development, 2003, 130(24): 6001−6012.[DOI] 16 Xiong Y, Liu T, Tian C, Sun S, Li J, Chen M. Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol, 2005, 59(1): 191−203.[DOI] 17 Maes T, van de Steene N, Zethof J, Karimi M, D'Hauw M, Mares G, van Montagu M, Gerats T. Petunia AP2-like genes and their role in flower and seed development. Plant Cell, 2001, 13(2): 229−244.[DOI] 18 Keck E, McSteen P, Carpenter R, Coen E. Separation of genetic functions controlling organ identity in flowers. EMBO J, 2003, 22(5): 1058−1066.[DOI] 19 Shigyo M, Ito M. Analysis of gymnosperm two-AP2-domain-containing genes. Dev Genes Evol, 2004, 214(33): 105−114.[DOI] 20 Nilsson L, Carlsbecker A, Sundas-Larsson A, Vahala T. APETALA2 like genes from Picea abies show functional similarities to their Arabidopsis homologues. Planta, 2007, 225(3): 589−602.[DOI] 21 Nei M, Rooney AP. Concerted and birth-and-death evolution of multigene families. Ann Rev Genet, 2005, 22(15): 121−152.[DOI] 22 Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res, 1997, 25(24): 4876−4882.[DOI] 23 Kumar S, Tamura K, Nei M. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform, 2004, 5(2): 150−163.[DOI] 24 Li GS, Meng Z, Kong HZ, Chen ZD, Theissen G, Lu AM.

Characterization of candidate class A, B and E floral homeotic genes from the perianthless basal angiosperm Chloranthus spicatus (Chloranthaceae). Dev Genes Evol, 2005, 215(9): 437−449.[DOI] 25 Nam J, Nei M. Evolutionary change of the numbers of homeobox genes in bilateral animals. Mol Biol Evol, 2005, 22(12): 2386−2394.[DOI] 26 Chuck G, Meeley RB, Hake S. The control of maize spikelet meristem fate by the APETALA2-like gene INDETERMINATE SPIKELET1. Genes Dev, 1998, 12(8): 1145−1154.[DOI] 27 Malcomber ST, Kellogg EA. Heterogeneous expression patterns and separate roles of the SEPALLATA gene LEAFY HULL STERILE1 in grasses. Plant Cell, 2004, 16(77): 1692−1706.[DOI] 28 Moose S, Sisco P. GLOSSY15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. Genes Dev, 1996 10(23): 3018−3027. 29 Lauter N, Kampani A, Carlson S, Goebel M, Moose SP. microRNA172 down-regulates GLOSSY15 to promote vegetative phase change in maize. Proc Natl Acad Sci USA, 2005, 102(26): 9412−9417.[DOI] 30 Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ. Molecular and genetic analyses of the SILKY1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell, 2000, 5(3): 569−579.[DOI] 31 Kellogg EA. Evolutionary history of the grasses. Plant Physiol, 2001, 125(3): 1198−1205. 32 Simpson GG, Dean C. Arabidopsis, the rosetta stone of flowering time. Science, 2002, 296(5566): 285−289.[DOI]

分析水稻 APETALA2 类基因的系统发育和表达模式
唐美芳1, 李贵生2, 陈明生2
1.西北农林科技大学动物科技学院, 杨凌 712100; 2.中国科学院遗传与发育生物学研究所植物基因组学国家重点实验室和植物基因研究中心, 北京 100101 摘 要: 多基因家族经历着生与死的进化并因此有助于生物的创新性进化。APETALA2 类基因属于 AP2 转录因子家族中 euAP2 分支。该类基因具有特征性基元, 并存在于蕨类植物、裸子植物和被子植物中。系统发育分析表明这类基因经历了 生与死的进化。原位杂交和 RT-PCR 结果表明水稻的 5 个 APETALA2 类基因在表达模式上既是冗余又是不同的。根据基因 系统发育树和表达模式讨论了这些基因的功能。 关键词: 创新性进化; 基因重复; microRNA172 作者简介: 唐美芳(1982−), 女, 湖南人, 硕士, 研究方向: 植物遗传学。E-mail:

Shared By:
Description: the phylogeny and expression pattern of apetala2 like genes in rice