Review Article | Volume: 10, Issue: 1, January, 2020

A critical review on: Significance of floral homeotic APETALA2 gene in plant system

Pooja Sharma Raj Singh Nirmala Sehrawat   

Open Access   

Published:  Jan 03, 2020

DOI: 10.7324/JAPS.2020.101017
Abstract

Flower development is a complex procedure regulated by combinatorial factors, such as transcription factors, peptides, hormones, and small RNAs. One of the important gene determining the floral structure and floral meristem is APETALA2 (AP2) which belongs to a large family of transcription factors. AP2 contributes stochastically in signaling pathway in flower development and in various bioactive components synthesis. The presence of GbAP2 transcripts in live fossil Ginkgo biloba leaves and female strobili tissue showed that GbAP2 might be involved directly in leaf and female strobili development, whereas it may possible that GbAP2 indirectly involved in synthesis of bioactive compounds such as flavonoids, terpenoids, ginkgolides, and organic acids. Gingko or Ginkgo biloba is among the most popular plant used in United States. Bioactive compounds isolated from the ginkgo plant are thought to exhibit as antioxidant and antiplatelet activity. Due to the pleotropic nature of AP2, it is involved in various tissues such as regulating in floral pattern, stem cell maintenance, floral organ identity, floral meristem, leaves, development of stems, and seed development. AP2 also regulate number of downstream genes but its own expression is negatively regulated at translational or post-translational levels by miRNA172 which is a small RNA (22 bp) and binds to complementary region of AP2 transcript. Mutation in AP2 showed increases in seed size and seed mass, this property of AP2 could be used in medicinal plant to enhance the valuable product. Since AP2 is engaged in various pathways it is essential to compile the functioning in the form of presented manuscript, which discusses the structure and functioning of AP2. We likewise explain how AP2 involved in various expressions and its regulatory mechanism, especially in the plant.


Keyword:     APETALA2 transcription factor miRNA172 floral development RNA-induced silencing complex nitrogen use efficiency.


Citation:

Sharma P, Singh R, Sehrawat N. A critical review on: Significance of floral homeotic APETALA2 gene in plant system. J Appl Pharm Sci, 2020; 10(1):124–130.

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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INTRODUCTION

According to the ABCDE model, APETALA2 (AP2) gene belongs to Class A gene category primary in Arabidopsis, which is responsible for sepal and petal development. It is one of the significant genes responsible to determine the identity of four major floral organs. Any type of alteration in AP2 gene sequence could cause severe developmental defects, especially homeotic floral organ distortion where petals are replaced by carpels or carpelloids and petals to stamens. In the case of weak AP2 mutant plant, the leaves were replaced by sepals and petals by antheroid, whereas in strong AP2 mutant plant, carpelloid-like structures were formed in place of sepals, petals are demised, and the stamen number is reduced. In recent years, scientists pay more focus on RNA interference (RNAi) to characterize the gene function in model and cultivated plants. RNAi is a technique of gene editing which is based on post-transcriptional gene silencing in eukaryotes to modify the phenotypes. Various small interfering RNAs (siRNAs) and micro RNAs (miRNAs) molecules are characterized which involved in gene regulation in plants system at transcriptional as well as translational levels. A miR172, 22 bp in length showing similarity with the transcript of a floral homeotic gene AP2 and regulates its expression pleiotropically. The accumulation of enhanced miR172 showing the same floral defects as shown in loss-of-function AP2 mutants. In 2005, two scientists Axtell and Bartel were reported that miR172 regulates in flowering plants, ferns, and gymnosperms except lycopods and moss (Axtell and Bartel, 2005). Recently in monocotyledons, such as maize, barley, and rice have shown the functioning of miR172 in differential stage transition in flower development (Lauter et al., 2005; Nair et al., 2010; Zhu and Helliwell, 2011).

During flower development, a cassette of regulatory genes has been revealed, which works collectively to regulate the floral meristem and floral organogenesis. The identification of floral organ is regulating under the influence of consistent homeotic genes. Homeotic genes are the regulatory genes that direct the position and development of particular body segments or structures. AP2 is one of the important homeotic gene, which governs the determination of floral meristem and floral development. To differentiate the flowering genes, the ABC model was designed which further modified as the ABCDE model of flower development (Colombo et al., 1995; Haughn and Somerville, 1988; Pelaz et al., 2000). Various combinatorial interaction of homeotic genes involved in flower development. Floral genes based on the ABCDE model are categorized in five different classes, such as A, B, C, D, and E (Bowman et al., 1991). Class A genes (AP1, SQUA, and AP2) control sepal development in whorl 1. Class A genes overlap with Class B genes (PI and AP3) to promote petal formation in whorl 2. Class B and Class C (AG) genes involved in stamen formation in whorl 3, while Class C genes alone promote gynoecium development in whorl 4 (Fig. 1) To sustain the floral structure, Class A (AP2) and Class C (AG) genes act mutually but in antagonistic fashion. Thus, AP2 and AG gene transcription spatially restricted by the first two whorls and last two whorls, respectively.

AP2 is one of the significant genes known from the decades for governing floral meristematic and floral organ tissue determination (Bowman et al., 1989; 1993; Huala and Sussex 1992; Irish and Sussex 1990; Komaki et al., 1988; Kunst et al., 1989; Schultz and Haughn 1993; Shannon and Meekswagner 1993). The presence of AP2 transcripts in floral (sepal, petal, anther, ovule, and silique) as well as in vegetative tissues (root, leaf, shoot, and stem) showed the importance of AP2 gene in reproductive and vegetative tissues (Sharma et al., 2017). Since high level of AP2 protein was observed in vegetative tissue, but still there is no report on any defects in stem or leaf development. Consequently, loss-of-function completely distorts the structure of flower but leaf and root structure seems healthy (Bowman et al., 1989). Besides this, it is hypothesized the AP2 function in stem and leaf may be due to the genetically redundancy in Arabidopsis (Okamuro 1997).

Figure 1. Representation of class A, B, C, D, and E genes with their respective tissue in model flower (modified from Krizek and Fletcher, 2005).

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CLASSIFICATION AND STRUCTURAL ORGANIZATION OF AP2 GENE

Floral homeotic AP2 gene belongs to APETALA2/Ethylene Responsive Factor super family. The genes belong to this family are involved in primary and secondary metabolism regulation, growth, and development. It also involved in abiotic responses. AP2 itself is a transcription factor which represents 147, 157, 201, and 148 targets in Arabidopsis, rice, wheat, and soya bean, respectively (Nakano et al., 2006; Sahu et al., 2016; Yant et al., 2010; Zhang et al., 2008). Respective targets have been divided into three different classes based on the number of AP2 domains. Class I encodes a functional protein having two AP2 domains, for example AP2 (Jofuku et al., 1994), AINTEGUMENTA (ANT) (Elliott et al., 1996; Klucher et al., 1996), Glossy15 (GL15) (Moose and Sisco 1996), SlAP2a (Karlova et al., 2011), SHAT1, and BniAP2. Class II encodes a functional protein having single AP2 domain, for example Ethylene-Responsive-element-binding-Factor (ERFs) (Ohme-Takagi and Shinshi 1995), It is a mutation caused by transposon element (TINY) (Wilson et al., 1996), AtEBP (Buttner and Singh 1997), and ABI4 (Finkelstein et al., 1998) and a Class III includes Related to ABI3/VP (RAV) (Kagaya et al., 1999) encodes a protein having one AP2 associated with B3 DNA-binding domain (Giraudat et al., 1992). Some additional sequence conserved in plants genome belonging to the AP2/ Ethylene-Responsive-element-binding-Factor (ERF) family known as soloist (Licausi et al., 2010; Nakano et al., 2006; Zhuang et al., 2008).

Since 1994, it is known that transcription start site (TSS) of AP2 is positioned at 263 bp upstream to the start codon (Jofuku et al., 1994). Recently, it is confirmed that AP2 having multi-TSS site responsible for gene expression (Sharma et al., 2017). AP2 is regulated by nearly 7.5 Kb flanking region located at fifth chromosome in model plant (Arabidopsis) with gene id: AT4G36920. The structure of AP2 gene comprised 10 exons and 9 introns with a transcript ranges from 1,300 to 1,500 bp (Fig. 2). AP2 gene comprised two AP2 domains, which are essential for AP2 function. Each AP2 domain is comprised 68 amino acids, which is evolutionary conserved in plants as AP2-like proteins. There were two conserved sequence box within each AP2 domain. The first motif comprised 19–22 basic amino acids and a conserved Tyrosine-Arginine-Glycine motif (Basic amino acids) (YRG) amino acids motif whereas the second motif comprised 42–43 amino acids with 18 amino acids as a core region that forms an amphipathic α-helix, which is essential for AP2 functioning (Allen et al., 1998; Jofuku et al., 1994). The AP2-like proteins are also characterized by the presence of linker region that is comprised 25–26 highly conserved amino acids and lies between the two AP2 domains (Allen et al., 1998; Jofuku et al., 1994).

Figure 2. Structure of AP2 gene with 10 exon–9 intron boundaries with intergenic region and adjacent gene (AT4G36910) in reverse orientation.

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It was considered that AP2 domain presents within plant system only (Riechmann and Myerowitz, 1998) but computer-assisted study search that Histidine and Asparagine rich Asparagine- Histidines domain (HNH)-AP2 class of homing endonucleases were also present in Cyanobacterium (Trichodesmium erythraeum) and virus genome (Enterobacteria phage and Bacteriophage Felix) suggesting the horizontal transfer of Asparagine- Histidines domain (HNH)-AP2 from bacteria to plants. Furthermore, intron-less AP2/ Ethylene-Responsive-element-binding-Factor (ERF) supports the horizontal gene transfer responsible for AP2 domain evolved from prokaryotes (Magnani et al., 2004; Wessler, 2005; Wuitschick et al., 2004).

AP2 itself regulate various downstream gene expression since it belongs to a super family of transcription factors (Yant et al., 2010). It suppresses the transcription of SOC1 and AGAMOUS gene expression and promotes the floral repressor AGL15 and miR156 expression (Adamczyk et al., 2007, Wu et al., 2009). Moreover, AP2 is also involved at the level of translational regulation by miR172 (Aukerman and Sakai 2003). AP2 act pleiotropically and its transcripts have been detected in Arabidopsis in several developmental stages of reproductive as well as in vegetative tissue (Jofuku et al., 1994; Kinoshita et al., 2004; Ripolle et al., 2011; Sharma et al., 2017). Hybridization experiments also showed the presence of AP2 transcripts in various tissues, such as leaf, shoot, stem, root, floral meristem, sepals, petals, and seeds (Wollmann et al., 2010). An eFP Browser, online software was developed to detect the microarray studies and revealed the AP2 distribution from vegetative tissue to reproductive tissue (Winter et al., 2007) (Fig. 3a and b). SHAT1 is an AP2-like gene which expresses in abscission zone during spikelet development in rice. In addition to this, Cleistogamy1 (Cly1) is an important gene in barley which expresses itself in spike to promotes cleistogamy (Nair et al., 2010; Wang et al., 2015). Cly1 is a member of AP2 gene family, which contains two AP2 domains and miR172 complementary target sequences (Kim et al., 2006). AP2 gene isolated from several crop showing sequence similarity as shown in Figure 4. In Arabidopsis, a single copy is enough for floral development and floral specification; however, it is known in Antirrhinum (Keck et al., 2003); Petunia hybrida (Maes et al., 2001); Brassica rapa (Liu et al., 2013) showing two AP2-like genes. Brassica juncea which is a tetraploid having three copies of AP2 (Sharma et al., 2018) and tomato (Karlova et al., 2011) having five AP2 copies might be required for flower development.

Figure 3. (a) Representation of AP2 expression in vegetative and reproductive tissues in Arabidopsis using eFP Browser online software (b) Representation of level of AP2 expression in different tissue under different stages of Arabidopsis using in silico.

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Figure 4. Phylogenetic tree showing relationship of different AP2 gene family members (At-Arabidopsis thaliana Bn-Brassica nigra Zm-Zea mays Ta-Triticum Aestivum Os- Oriza sativum Sl- solenum lycopercicum Vr-Vigna radiata Rc Ricinus communis) using MEGA 6.0.

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SIGNIFICANT VALUE OF AP2 GENE IN PLANT SYSTEM

Several reports are available which reveals that AP2 play significant role in gene regulation (Jofuku et al., 1994; Ripoll et al., 2011). Due to the presence of cis-regulatory elements in both directions it is examined that the AP2 promoter transcribes the genes in both directions hence it is a bidirectional promoter which controls the pleotropic expression in plant developmental biology (Sharma et al., 2017). Moreover, the expression of AP2 is negatively regulated via miR172, which is nearly 22 bp in length, highly conserved, and non-coding RNA. Due to sequence-complementary, miR172 can easily bind to their targets site on AP2 transcript outside the AP2 domains. Thus, AP2 expression is regulated by miR172 through one of two or both mechanisms (translation inhibition and transcript cleavage) (Chen, 2004; Zhao et al., 2007). In Arabidopsis, the binding of miR172 to AP2 transcripts suppresses its expression (Chen, 2004; Zhu and Helliwell, 2011), whereas in barley miR172 digest the AP2 transcripts for negative regulation (Houston et al., 2013). The interaction between miR172 and AP2 transcripts shows that the miR172 regulate AP2 functioning in common bean or Phaseolus vulgaris (Nova-Franco et al., 2015). Some of the genetic modifications within miR172 sequences revealed that AP2-miR172 interaction plays an important role in regulating flowering time in gloxinia plants (Li et al., 2019). Expression of class A gene, such as AP2 transcripts, is reduced in transgenics by over-expression of miR172, which affects apple fruit weight (Yao et al., 2016). Hence, AP2 shows stochastic interaction between miR172-AP2, which is critical for proper floral differentiation and development.

Figure 5. Gene network highlighting the regulatory pathway of AP2 during stem cell maintenance and flower development.

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AP2 confers the place and timing of floral organs as well as floral meristem and specification development in plants. It directly promotes the Class C WUSCHEL gene (WUS) gene with down regulating the CLAVATA (CLV) gene to maintain the stem cell niche in floral meristem. However, WUS directly promotes the CLAVATA (CLV) gene and CLAVATA (CLV) represses the activity of WUS for feedback regulation as shown in Figure 5 (Lenhard et al., 2001; Wurschum et al., 2006). It also observed that ap2 mutant lines induced more hexose/sucrose ratios in seeds as compared with wild-type seeds (Ohto et al., 2005). Similarity, loss-of-function of BnAP2 gene showed defects in shape, structure, development, and size of seeds in Brassica nigra (Yan et al., 2012) and RcAP2 gene in Rosa Chinensis regulates the number of rose petals (Han et al., 2018). Different splice variant of HvAP2 revealed the differences in size and shape of barley inflorescence (Houston et al., 2013). Hence, AP2 is an essential gene in length of internode in inflorescence, seed size, and seed mass. However, it could be one of the important genes, which regulate the cascade pathway in floral development in medicinal plant. AP2 transcript in Arabidopsis distorts the developmental changes, such as petals to carpels transition and petals to stamens transition in the outer two whorls of flower structure (Table 1). Furthermore, AP2 regulates replum formation during developing fruit in Arabidopsis (Ripoll et al., 2011). SiAP2, an ortholog of AP2 in tomato involved in ethylene biosynthetic process to confers the fruit ripening (Chung et al., 2010; Rumyana et al., 2011).

Ongoing investigation uncovers that the density of grains in barley inflorescence changes as the interaction between alleles of HvAP2 transcript and miR172 differs (Houston et al., 2013). Thus, the variation in HvAP2 transcripts and miR172 interaction showed that both are involved in the regulation of size and shape of barley inflorescence. Similarly, in Phaseolus vulgaris, legume-rhizobia nitrogen-fixing symbiosis system is also influenced by miRNA172-AP2-1 complex (Nova-Franco et al., 2015).

Table 1. AP2 mutations observed in different whorl of flower in Arabidopsis.



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IMPORTANCE OF AP2 GENE IN CROP IMPROVEMENT

AP2/ Ethylene-Responsive-element-binding-Factor (ERF) is a super known family, which regulates stress signaling, floral meristem, and floral developmental genes. In rice, over-expression of OsAP37 and OsERF71 genes showed more tolerance against drought, which provides more seed yield (Lee et al., 2016; Oh et al., 2009). OsERF71 is an important gene, which further activates various stress responsive genes, and lignin biosynthesis associated genes causing changes in structure of root. In addition to this, another important AP2 gene (EjAP2-1) characterized from Eriobotrya japonica regulates fruit lignification, which is induced by chilling injury (Zeng et al., 2015). Due to these biotic and abiotic environmental factors, productivity of crop is severely affected. Over the last decade, it was observed that the AP2 candidates play an important role in nitrogen use efficiency (NUE) and plant response toward various abiotic factors. Sixteen AP2 family members were reported as nitrogen deficient responsive genes, which expressed in roots and leaf tissue of rice (Obertello et al., 2015; Yang et al., 2015). Similarly, finding of more nitrogen responsive genes could be beneficial for biological nitrogen fixation in cereal crops using available sequenced databases. NUE depends upon capability of nitrogen uptake by healthy plants under normal condition, which are utilized by the plant for their optimum growth and development (Bi et al., 2009). Due to various factors, the NUE may vary in crop to crop or within the same crop. Furthermore, the stochastic pathways behind nitrogen deficient and nitrogen induced genes may improve the NUE and decreases the unnecessary use of synthetic nitrogen fertilizers for sustainable agriculture.


PHARMACEUTICAL VALUE OF AP2

AP2 is a well-known gene for its pleotropic expression in vegetative as well as in reproductive tissues in plant system (Sharma et al., 2017). It was found that AP2 contributes stochastically in signaling pathway of various bioactive compounds synthesis, which has huge importance in pharmaceutical industry (Phukan et al., 2017; Udomsom et al., 2016; Xu et al., 2016). Total 171 AP2 members were involved in biosynthesis of bioactive compounds (tanshinone and phenolic acid) characterized from Salvia miltiorrhiza which is used in the treatment of cardiovascular disease in Asia, United States, and several European countries and have more pharmaceutical values. Moreover, the medicine exhibits many other activities such as neuroprotective, anti-inflammatory, antioxidant, and strong antidementia (Ji et al., 2016; Xu et al., 2016). AP2 transcription factors from Ophiorrhiza pumila also regulating camptothecin alkaloid, which is used as an initiator in the synthesis of chemotherapeutic drugs (Udomsom et al., 2016). In Artemisia annua, AP2/ERF transcription factor family were also involved in artimisinin and artemisinic acids biosynthesis, which is commonly used in antimalarial drug and further explored for antiviral, anticancerous and antischistosomal drugs (Afrin et al., 2015). In tobacco and Catharanthus roseus, one of the AP2/ERF family members (GLYCOALKALOID METABOLISM 9) was involved in regulation of toxic alkaloid production which is considered as antinutritional compounds (Cárdenas et al., 2016).

In addition to this, AP2 mutant showed rapid endosperm growth (Zhang et al., 2018), increase in seed size, and seed mass (Ohto et al., 2009), this property of AP2 could be used in medicinal plant using genetic engineering to enhance the valuable product. The novel approach may prove to be beneficial to enhance the inflorescence, seed, and oil production of pharmaceutical important plants.


CONCLUSION

AP2 plays a pivotal role in gene expression regulation of many plant developmental processes. Recently, miR172-AP2 complex is revealed as an essential regulator in nitrogen-fixing symbiosis and nodulation in legumes. The study could reveal new opportunities in biological nitrogen fixation in cereal crops, which may reduce the gradual use of synthetic nitrogen in agriculture system and improve the NUE. Since the AP2 influences the seed mass as well as seed size, it could directly control seed mass and seed size and may prove to be beneficial for oil plants and cereals for more inflorescence. Moreover, AP2 regulate signaling pathway in biosynthesis of tanshinone and phenolic, which is a traditional Chinese medicine and have high pharmaceutical values. During these stochastic processes, several factors are unclear. It seems highly probable that these regulators should further empirically studied to understand the whole processing.


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Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature, 2000; 405:200–3.

Phukan UJ, Jeena GS, Tripathi V, Shukla RK. Regulation of Apetala2/Ethylene response factors in plants. Front Plant Sci. 2017; 21(8):150.

Riechmann JL, Meyerowitz EM. The AP2/EREBP family of plant transcription factors. Biol Chem, 1998; 379:633–46.

Ripoll JJ, Roeder AH, Ditta GS, Yanofsky MF. A novel role for the floral homeotic gene APETALA2 during Arabidopsis fruit development. Development, 2011; 138:5167–76.

Sahu R, Sharaff M, Pradhan M, Sethi A, Bandyopadhyay T, Mishra VK, Chand R, Chowdhury AK, Joshi AK, Pandey SP. Elucidation of defense-related signaling responses to spot blotch infection in bread wheat (Triticum aestivum L.). Plant J, 2016; 86:35–49.

Schultz EA, Haughn GW. Genetic analysis of the floral initiation process (FLIP) in Arabidopsis. Development, 1993; 119:745–65.

Shannon S, Meeks-Wagner DR. Genetic interactions that regulate inflorescence development in Arabidopsis. Plant Cell, 1993; 5:639–55.

Sharma P, Kumar V, Singh SK, Thakur S, Siwach P, Sreenivasulu Y, Srinivasan R, Bhat SR. Promoter trapping and deletion analysis show arabidopsis thaliana apetala2 gene promoter is bidirectional and functions as a pollen and ovule-specific promoter in the reverse orientation. Appl Biochem Biotechnol, 2017; doi:10.1007/s12010-017-2420-9

Sharma P, Watts A, Kumar V, Srinivasan R, Siwach P. Cloning, characterization and expression analysis of APETALA2 genes of Brassica juncea (L.) Czern. Indian J Exp Biol, 2018; 56:604–10.

Udomsom N, Rai A, Suzuki H, Okuyama J, Imai R, Mori T, Nakabayashi R, Saito K, Yamazaki M. Function of AP2/ERF transcription factors involved in the regulation of specialized metabolism in Ophiorrhiza pumila revealed by transcriptomics and metabolomics. Frontiers Plant Sci, 2016; 7:1861.

Wang N, Ning SZ, Wu JZ, Tagiri A, Komatsuda T. An epiallele at cly1 affects the expression of floret closing (Cleistogamy) in barley. Genetics, 2015; 199:95–104; doi:10.1534/genetics.114.171652

Wessler SR. Homing into the origin of the AP2 DNA binding domain. Trends Plant Sci, 2005; 10(2):54–6.

Wilson K, Long D, Swinburne J, Coupland G. A Dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell, 1996; 8:659–71.

Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ. An electronic fluorescent pictograph browser for exploring and analyzing large-scale biological data sets. PLoS One, 2007; 2:e718.

Wollmann H, Mica E, Todesco M, Long JA, Weigel D. On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development, 2010; 137:3633–42.

Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell, 2009; 138(4):750–9.

Wuitschick JD, Lindstrom PR, Meyer AE, Karrer KM. Homing endonucleases encoded by germ line-limited genes in Tetrahymena thermophile have APETELA2 DNA binding domains. Eukaryotic Cell, 2004; 685–694; doi:10.1128/EC.3.3.685-694.2004

Wurschum T, Gross-Hardt R, Laux T. APETALA2 regulates the stem cell niche in the Arabidopsis shoot meristem. Plant Cell, 2006; 18:295–307.

Xu H, Song J, Luo H, ZhangY, Li Q, ZhuY, Xu J, Li Y, Song C, Wang B, Sun W, Shen G, Zhang X, Qian J, Ji A, Xu Z, Luo X, He L, Li C, Sun C, Yan H, Cui G, Li X, Li X, Wei J, Liu J, Wang Y, Hayward A, Nelson D, Ning Z, Peters RJ, Qi X, Chen S. Analysis of the genome sequence of the medicinal plant Salvia miltiorrhiza. Mol Plant, 2016; 9:949–952; doi:10.1016/j.molp.2016.03.010

Yan X, Zhang L, Chen B, Xiong Z, Chen C, Wang L, Yu J, Lu C, Wei W. Functional identification and characterization of the Brassica napus transcription factor gene BnAP2, the ortholog of Arabidopsis thaliana APETALA2. PLoS One, 2012; 7:e33890; doi:10.1371/journal.pone.0033890

Yang W, Yoon J, Choi H, Fan Y, Chen R, An G. Transcriptome analysis of nitrogen-starvation-responsive genes in rice. BMC Plant Biol, 2015; 15:31.

Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, Wollmann H, Chen X, Schmid M. Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell, 2010; 22:2156–70.

Yao JL, Tomes S, Xu J, Gleave AP. How microRNA172 affects fruit growth in different species is dependent on fruit type. Plant Signal Behav, 2016; 11:e1156833.

Zeng JK, Li X, Xu Q, Chen JY, Yin XR, Ferguson IB, Chen KS. EjAP2-1, an AP2/ERF gene, is a novel regulator of fruit lignification induced by chilling injury, via interaction with EjMYB transcription factors. Plant Biotechnol J, 2015; 13:1325–34.

Zhang G, Chen M, Chen X, Xu Z, Guan S, Li LC, Li A, Guo J, Mao L, Ma Y. Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J Exp Bot, 2008; 59:4095–107.

Zhao L, Kim Y, Dinh TT, Chen X. miR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. Plant J, 2007; 51:840–9.

Zhu QH, Helliwell CA. Regulation of flowering time and floral patterning by miR172. J Exp Bot, 2011; 62:487–95.

Zhuang J, Cai B, Peng RH, Zhu B, Jin XF, Xue Y, Gao F, Fu XY, Tian YS, Zhao W, Qiao YS, Zhang Z, Xiong AS, Yao QH. Genome-wide analysis of the AP2/ERF gene family in Populus trichocarpa. Biochem Biophys Res Commun, 2008; 371:468–74.

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Ohto MA, Floyd SK, Fischer RL, Goldberg RB, Harada JJ. Effects of APETALA2 on embryo, endosperm, and seed coat development determine seed size in Arabidopsis. Sex Plant Reprod, 2009; 22(4):277-89. https://doi.org/10.1007/s00497-009-0116-1

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; 94:7076-81. https://doi.org/10.1073/pnas.94.13.7076

Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature, 2000; 405:200-3. https://doi.org/10.1038/35012103

Phukan UJ, Jeena GS, Tripathi V, Shukla RK. Regulation of Apetala2/Ethylene response factors in plants. Front Plant Sci. 2017; 21(8):150. https://doi.org/10.3389/fpls.2017.00150

Riechmann JL, Meyerowitz EM. The AP2/EREBP family of plant transcription factors. Biol Chem, 1998; 379:633-46.

Ripoll JJ, Roeder AH, Ditta GS, Yanofsky MF. A novel role for the floral homeotic gene APETALA2 during Arabidopsis fruit development. Development, 2011; 138:5167-76. https://doi.org/10.1242/dev.073031

Sahu R, Sharaff M, Pradhan M, Sethi A, Bandyopadhyay T, Mishra VK, Chand R, Chowdhury AK, Joshi AK, Pandey SP. Elucidation of defense-related signaling responses to spot blotch infection in bread wheat (Triticum aestivum L.). Plant J, 2016; 86:35-49. https://doi.org/10.1111/tpj.13149

Schultz EA, Haughn GW. Genetic analysis of the floral initiation process (FLIP) in Arabidopsis. Development, 1993; 119:745-65.

Shannon S, Meeks-Wagner DR. Genetic interactions that regulate inflorescence development in Arabidopsis. Plant Cell, 1993; 5:639-55. https://doi.org/10.2307/3869807

Sharma P, Kumar V, Singh SK, Thakur S, Siwach P, Sreenivasulu Y, Srinivasan R, Bhat SR. Promoter trapping and deletion analysis show arabidopsis thaliana apetala2 gene promoter is bidirectional and functions as a pollen and ovule-specific promoter in the reverse orientation. Appl Biochem Biotechnol, 2017; doi:10.1007/s12010-017-2420-9 https://doi.org/10.1007/s12010-017-2420-9

Sharma P, Watts A, Kumar V, Srinivasan R, Siwach P. Cloning, characterization and expression analysis of APETALA2 genes of Brassica juncea (L.) Czern. Indian J Exp Biol, 2018; 56:604-10.

Udomsom N, Rai A, Suzuki H, Okuyama J, Imai R, Mori T, Nakabayashi R, Saito K, Yamazaki M. Function of AP2/ERF transcription factors involved in the regulation of specialized metabolism in Ophiorrhiza pumila revealed by transcriptomics and metabolomics. Frontiers Plant Sci, 2016; 7:1861. https://doi.org/10.3389/fpls.2016.01861

Wang N, Ning SZ, Wu JZ, Tagiri A, Komatsuda T. An epiallele at cly1 affects the expression of floret closing (Cleistogamy) in barley. Genetics, 2015; 199:95-104; doi:10.1534/genetics.114.171652 https://doi.org/10.1534/genetics.114.171652

Wessler SR. Homing into the origin of the AP2 DNA binding domain. Trends Plant Sci, 2005; 10(2):54-6. https://doi.org/10.1016/j.tplants.2004.12.007

Wilson K, Long D, Swinburne J, Coupland G. A Dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell, 1996; 8: 659-71. https://doi.org/10.1105/tpc.8.4.659

Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ. An electronic fluorescent pictograph browser for exploring and analyzing large-scale biological data sets. PLoS One, 2007; 2:e718. https://doi.org/10.1371/journal.pone.0000718

Wollmann H, Mica E, Todesco M, Long JA, Weigel D. On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development, 2010; 137:3633-42. https://doi.org/10.1242/dev.036673

Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell, 2009; 138(4):750-9. https://doi.org/10.1016/j.cell.2009.06.031

Wuitschick JD, Lindstrom PR, Meyer AE, Karrer KM. Homing endonucleases encoded by germ line-limited genes in Tetrahymena thermophile have APETELA2 DNA binding domains. Eukaryotic Cell, 2004; 685-694; doi:10.1128/EC.3.3.685-694.2004 https://doi.org/10.1128/EC.3.3.685-694.2004

Wurschum T, Gross-Hardt R, Laux T. APETALA2 regulates the stem cell niche in the Arabidopsis shoot meristem. Plant Cell, 2006; 18:295-307. https://doi.org/10.1105/tpc.105.038398

Xu H, Song J, Luo H, ZhangY, Li Q, ZhuY, Xu J, Li Y, Song C, Wang B, Sun W, Shen G, Zhang X, Qian J, Ji A, Xu Z, Luo X, He L, Li C, Sun C, Yan H, Cui G, Li X, Li X, Wei J, Liu J, Wang Y, Hayward A, Nelson D, Ning Z, Peters RJ, Qi X, Chen S. Analysis of the genome sequence of the medicinal plant Salvia miltiorrhiza. Mol Plant, 2016; 9:949-952; doi:10.1016/j.molp.2016.03.010 https://doi.org/10.1016/j.molp.2016.03.010

Yan X, Zhang L, Chen B, Xiong Z, Chen C, Wang L, Yu J, Lu C, Wei W. Functional identification and characterization of the Brassica napus transcription factor gene BnAP2, the ortholog of Arabidopsis thaliana APETALA2. PLoS One, 2012; 7:e33890; doi:10.1371/journal. pone.0033890 https://doi.org/10.1371/journal.pone.0033890

Yang W, Yoon J, Choi H, Fan Y, Chen R, An G. Transcriptome analysis of nitrogen-starvation-responsive genes in rice. BMC Plant Biol, 2015; 15:31. https://doi.org/10.1186/s12870-015-0425-5

Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, Wollmann H, Chen X, Schmid M. Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell, 2010; 22:2156-70. https://doi.org/10.1105/tpc.110.075606

Yao JL, Tomes S, Xu J, Gleave AP. How microRNA172 affects fruit growth in different species is dependent on fruit type. Plant Signal Behav, 2016; 11:e1156833. https://doi.org/10.1080/15592324.2016.1156833

Zeng JK, Li X, Xu Q, Chen JY, Yin XR, Ferguson IB, Chen KS. EjAP2-1, an AP2/ERF gene, is a novel regulator of fruit lignification induced by chilling injury, via interaction with EjMYB transcription factors. Plant Biotechnol J, 2015; 13:1325-34. https://doi.org/10.1111/pbi.12351

Zhang G, Chen M, Chen X, Xu Z, Guan S, Li LC, Li A, Guo J, Mao L, Ma Y. Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J Exp Bot, 2008; 59: 4095-107. https://doi.org/10.1093/jxb/ern248

Zhao L, Kim Y, Dinh TT, Chen X. miR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. Plant J, 2007; 51:840-9. https://doi.org/10.1111/j.1365-313X.2007.03181.x

Zhu QH, Helliwell CA. Regulation of flowering time and floral patterning by miR172. J Exp Bot, 2011; 62:487-95. https://doi.org/10.1093/jxb/erq295

Zhuang J, Cai B, Peng RH, Zhu B, Jin XF, Xue Y, Gao F, Fu XY, Tian YS, Zhao W, Qiao YS, Zhang Z, Xiong AS, Yao QH. Genome-wide analysis of the AP2/ERF gene family in Populus trichocarpa. Biochem Biophys Res Commun, 2008; 371:468-74. https://doi.org/10.1016/j.bbrc.2008.04.087

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