Research paperGenome-wide identification and expression of YABBY genes family during flower development in Punica granatum L.
Introduction
The YABBY is unique transcription factor in plants, belonging to the zinc finger protein superfamily. YABBY proteins have two highly conserved domains: N-terminal C2C2 type zinc finger domain and C-terminal YABBY domain (Golz et al., 2004, Sieber et al., 2004). The YABBY transcription factors play significant roles in regulation of diverse developmental processes, such as formation of adaxial-adaxial polarity, lamina expansion and floral organ development (Eckardtn, 2010, Ha et al., 2010, Tanaka et al., 2012). It has been reported that the YABBY play different roles in lateral organ development, such as leaves (Eckardtn, 2010, Ha et al., 2010), floral organs (Yamada et al., 2011, Tanaka et al., 2012, Fourquin et al., 2014) and fruit development (Han et al., 2015).
The YABBY transcription factors have been extensively studied in dicotyledon plant. There are six YABBY members in Arabidopsis, YABBY1 (FIL, FILAMENTOUS FLOWER), YABBY2 (YAB2), YABBY3 (YAB3), YABBY4 (INO, INNER NO OUTER), YABBY5 (YAB5), and CRC (CRABS CLAW). FIL, YAB2 and YAB3 are always expressed in the primordia of lateral organs, which determine the abaxial cell fates (Siegfried et al., 1999) and participate in floral organ formation and leaf development (Sawa et al., 1999, Eshed et al., 2004, Stahle et al., 2009), and they act redundantly to promote vegetative organ development (Bowman, 2000, Eckardtn, 2010, Sarojam et al., 2010). INO and CRC are expressed in specific tissues: INO participates in the development of ovule outer integument, while CRC have been reported to be associated with polarity of nectary and carpel (Bowman and Smyth, 1999, Zhang et al., 2013). Twenty-three YABBY genes have been identified in cotton (Gossypium hirsutum). All GhYABBYs are expressed in bud, flower and stem meristem tissues. The YABBY genes in cotton may be involved in the development of above-mentioned tissues (Xu et al., 2015). In tomato (Solanum lycopersicum), nine YABBY genes have been located on 7 chromosomes. The expression pattern of SlYABBY is similar to that of Arabidopsis (Huang et al., 2013). As a homolog of INO, LeYABBYB have been cloned from tomato, which is critical for the development of abaxial cells of leaf primordium (Kim et al., 2003). Cong et al. (2008) found that FAS protein was encoded by a YABBY-like gene in tomato, which mainly regulated the number of carpels during flowering and fruit development. Bartley and Ishida, 2002, Bartley and Ishida, 2003, Bartley and Ishida, 2007 found that LeYAB2, independent of ethylene signaling pathway, was induced by low temperature to express in sepals of cv.VFNT cherry tomato. LeYAB2 is highly expressed in the epidermis of tomato fruit during ripening period, suggesting that LeYAB2 may affect the abaxial cell of pericarp and act a pivotal part in fruit ripening. Previous studies proved that homologous gene YABBY5 played a key role in regulating the fruit morphogenesis of Fingered Citron (Citrus medica L. var. sarcodactylis Swingle) (Han, 2014). CmsYABBY5 is highly expressed in pistils and stamens of Fingered Citron, but it is significantly low expressed in leaves. It suggests that CmsYABBY5 may be involved in pistil and stamen development of Fingered Citron (Liao et al., 2016).
Many YABBY genes have been studied in monocotyledon plants, such as Oryza sativa, Zea mays and Triticum aestivum (Zhao et al., 2006). Thirteen YABBY genes have been described in the maize genome (Ge et al., 2014), eight YABBY genes in rice (Toriba et al., 2007). OsYABBY4 play a critical role in the development of vascular structure (Liu et al., 2007), DL (DROOPING LEAF) is orthologous with CRC, which is mainly related to the formation of leaf midvein and flower development in rice (Yamaguchi et al., 2004). In dl mutant, carpel is transformed to stamen (Toriba et al., 2007). OsYAB1 has high homology with AtYAB2 and AtYAB5, it participates in the development of stamen, carpel and meristem (Toriba et al., 2007). Tanaka et al. (2017) found that OsTOB1, OsTOB2 and OsTOB3 were orthologous with FIL, which participated in the development of reproductive meristem. OsTOB1 acts a vital role to promote development of lateral organs and maintenance of meristem in rice spikelets (Tanaka et al., 2012). OsYAB3 participates in the development of leaves, while OsYAB4 is mainly expressed in rice vascular system (Dai et al., 2007, Liu et al., 2007). Juarez et al. (2004) cloned zyb9 and zyb14 of maize, based on conservative domain sequences of FIL, YAB2 and YAB3. zyb9 and zyb14 are expressed only in the paraxial surface of leaf primordia. Subcellular localization analysis showed that TaYAB1 and TaCRC fusion protein were localized in the nucleus, and they might play a key role in transcription and transcriptional regulation during the process of wheat dorsoventral polarity (Zhao et al., 2009). Evolutional study in plants showed that YABBY genes have not been found in bryophytes and lycopodialeo genomes, suggesting the YABBY is a unique transcription factor for seed plants (Finet et al., 2016).
Pomegranate is an important commercial fruit tree, which are widely grown in tropics and subtropics areas. There are bisexual flowers (vase shape) and functional male flowers (bell shape) in pomegranate. Ovule sterility causes functional male flowers which fall off after flowering and seriously affects fruit yield (Wetzstein et al., 2013, Chen et al., 2017a, Chen et al., 2017b). The genome data provide critical support for the function research of pomegranate gene (Qin et al., 2017, Yuan et al., 2018). In this study, the YABBY genes were identified in pomegranate. PgYABBY genes were computationally and experimentally characterized. A comparison of expression patterns with flowers in development stages were studied in the bisexual and functional male flowers of pomegranate. Our results have potential significance for the function research of PgYABBY genes.
Section snippets
Plant material and data collection for expression analysis
From April to June 2018, the bisexual flowers and functional male flowers of pomegranate were collected at Baima Base for Teaching and Scientific Research of Nanjing Forestry University. Flowers were categorized into eight stages according to their vertical diameter: 3.0–5.0 mm (P1), 5.1–8.0 mm (P2), 8.1–10.0 mm (P3), 10.1–12.0 mm (P4), 12.1–14.0 mm (P5), 14.1–16.0 mm (P6), 16.1–18.0 mm (P7), and 18.1–20.0 mm (P8) (Fig. 1). Three biological repeats were set up at each stage. Samples were frozen
Identification and sequence analysis of YABBY transcription factor
A total of 6 PgYABBY genes were identified in pomegranate using two methods of local blast and hmmsearch model. All candidate proteins were confirmed to belong to YABBY family.
The physicochemical properties of PgYABBY amino acid sequences were analyzed by ExPASy Proteomics Server. The results showed that the length of coding region of 6 PgYABBY genes ranged from 507 bp (PgCRC) to 675 bp (PgYAB3) (Table 3). The numbers of amino acids translated by YABBY varied from 168 aa to 224 aa, and the
Discussion
The YABBY family is a plant-specific transcription factor, with the typical zinc-finger and YABBY conserved domain. YABBY family genes play important regulatory roles in the development of lateral organs and abaxial-adaxial polarity. Many YABBY genes are identified in plants, with a large variable among species. For example, six AtYABBY genes have been identified in Arabidopsis, eight OsYABBY genes in rice (Toriba et al., 2007), twenty-three GhYABBY genes in cotton (Xu et al., 2015), thirteen
Conclusion
In this study, six YABBY genes were identified in pomegranate. PgYABBY genes were computationally and experimentally characterized through systematical analysis of gene structure, function and evolution. Our results illustrated the dynamic transcription patterns of PgYABBYs during flower development, indicating that PgINO might participate in the differentiation of flower organs in pomegranate.
CRediT authorship contribution statement
Yujie Zhao: Conceptualization, Methodology, Writing - original draft. Cuiyu Liu: Visualization. Dapeng Ge: Visualization, Investigation. Ming Yan: Methodology, Validation. Yuan Ren: . Xianbin Huang: . Zhaohe Yuan: Project administration, Supervision.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We thank Honglian Zhao and Dr. Yuying Wang for technical assistance and comments. This work was supported by the Initiative Project for Talents of Nanjing Forestry University [GXL2014070, GXL2018032], the Priority Academic Program Development of Jiangsu High Education Institutions [PAPD], and the Natural Science Foundation of Jiangsu Province [BK20180768].
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