Genome-wide identification, characterization and expression analysis of NF-Y gene family in relation to fruit ripening in banana
Introduction
Banana (Musa acuminata) is a major staple food and export product in many countries, with an annual output of more than 100 million tons worldwide (http://faostat.fao.org). Banana is a typical climacteric fruit that undergo rapid ripening process after harvest, including climacteric respiration, pulp softening, peel de-greening, and production of aroma compounds. Postharvest ripening is important for the formation of commercial quality of the fruit. However, over-ripening is undesirable, which reduces marketability and decrease disease resistance. Therefore, a better understanding of fruit ripening and senescence may benefit the development of strategies to improve the sensorial quality and reduce post-harvest fruit losses.
Transcriptional regulation plays a vital role in plant growth and development. Fruit ripening and senescence is the late stage of plant development. An increasing of transcription factors have been reported to be involved in regulation of fruit ripening and senescence (Gao et al., 2015; Li et al., 2018, 2016b; Weng et al., 2015; Zhu et al., 2014). Recently, several transcription factors have also been identified as ripening regulators in harvested banana fruit. Han et al. (2016) reported that MaERF11 transcription factor recruits histone deacetylase MaHDA1 and represses the expression of MaACO1 and expansins during banana fruit ripening. Kuang et al. (2017) showed that MaDREB2 may serve as both transcriptional activator and repressor to participate in the regulation of ripening-related genes in harvested banana fruit ripening. Xiao et al. (2018) proposed that MabHLH6 may act as a positive regulator of starch degradation at transcriptional and translational levels via direct activation of a series of starch degradation-related genes. Elitzur et al. (2016) confirmed that MaMADS transcription factors are necessary for banana fruit ripening by antisense or RNA interference technology. Therefore, banana fruit ripening is the result of transcriptional regulation by multiple transcription factors. Considering the complex nature of fruit ripening, only a limited number of transcription factors associated with fruit ripening have been identified in banana.
Nuclear factor Y (NF-Y), also termed as Heme activator protein (HAP) and CCAAT-box binding factor (CBF), is widespread in higher eukaryotes (Zhao et al., 2016). NF-Y is a heterotrimeric transcription factor consisting of distinct subunits: NF-YA (HAP2/CBF-B), NF-YB (HAP3/CBF-A) and NF-YC (HAP5/CBF-C) (Mantovani, 1999). In yeast and mammals, each subunit of NF-Y is encoded by a single gene which have multiple splicing forms or undergo various post-translational modifications (Li et al., 1992; Mantovani, 1999). In plants, each subunit of NF-Y is encoded by multiple genes, which further form different sub-families (Petroni et al., 2012). Individual subunit cannot independently regulate transcription; instead, they must function in heterotrimers (Zhao et al., 2016). NF-YB and NF-YC form a heterodimer via their conserved Histone Fold Domains, which is then bound by NF-YA to form a NF-YA/NF-YB/NF-YC complex (Gnesutta et al., 2017; Nardone et al., 2017). The recognition and binding of NF-YA to the CCAAT cis-element and the transcriptional activation or inhibition activities of NF-YB/NF-YC confer the heterotrimeric complex to function as a transcription factor. In addition, subunits of NF-Y also interact with other transcription factors to regulate expression of target genes (Cao et al., 2014; Huang et al., 2015; Xu et al., 2016; Yamamoto et al., 2009). NF-Ys play important roles in plant growth, development and stress responses, including embryo development, seed dormancy and germination, hypocotyl elongation, photomorphogenesis, root growth, flowering, abiotic stress and plant-microbe interactions (Eugenia Zanetti et al., 2017; Swain et al., 2017; Zhao et al., 2016). Unfortunately, little is known about the role of NF-Y in ripening and senescence regulation of harvested fruit.
The objective of the present study was to investigate the potential functions of NF-Y transcription factors in regulating ripening of harvested banana fruit. A total of 44 NF-Y genes (14 MaNF-YA, 16 MaNF-YB, and 14 MaNF-YC) were isolated and characterized from the banana genome. Furthermore, tissue-specific expression patterns of the 44 MaNF-Y genes, and the transcript levels of 20 selected MaNF-Y genes in peel and pulp of harvested banana fruit with three different ripening characteristics, including natural ripening, ethylene-induced ripening and 1-MCP-delayed ripening, were investigated by qRT-PCR. Our results provided a set of candidate NF-Y genes to further study transcriptional regulation of ripening in harvested banana fruit.
Section snippets
Materials and treatments
Hands of green mature banana (Musa acuminata cv. Brazil) were obtained from a local orchard in Guangzhou. Fruit were selected for uniformity of shape, color, and absence of blemishes or disease. Fruit were cut into fingers and then dipped for 3 min in 0.1% Sportak1 (prochloraz, Bayer) fungicide solution to control the postharvest diseases, and then air-dried. The fruit were divided randomly into three groups. The first group and the second group, respectively, were fumigated with 0.5 mL L−1 C2H4
Isolation and characterization of MaNF-Y family genes in banana
After removing the redundant sequences, 44 MaNF-Y genes were identified and isolated from banana fruit, including 14 MaNF-YAs, 16 MaNF-YBs and 14 MaNF-YCs (Table S2). Their full length cDNA were cloned and confirmed by sequencing. The length of MaNF-Y proteins were identical to the genome except MaNF-YA2 which had more than four amino acids (DLVS). Five MaNF-YAs, one MaNF-YB and four MaNF-YCs had one or two base mutation compared to the sequence retrieved from the banana genome, resulting in
Discussion
NF-Y is a trimeric transcription factor complex present in eukaryotes, consisting of NF-YA, NY-YB and NF-YC subunits. In plants, each subunit of NF-Y is encoded by multiple genes (Petroni et al., 2012). There are 36 NF-Y members (10 NF-YA, 13 NF-YB, and 13 NF-YC) in Arabidopsis thaliana(Siefers et al., 2009), 34 NF-Y members (11 NF-YA, 11 NF-YB, and 12 NF-YC) in Oryza sativa (Yang et al., 2017), 59 NF-Y members (10 NF-YA, 29 NF-YB, and 20 NF-YC) in Solanum lycopersicum (Li et al., 2016a), 34
Conclusion
In this study, we identified and confirmed a total of 44 NF-Y genes from banana genome, including 14 MaNF-YA, 16 MaNF-YB, and 14 MaNF-YC, which were distributed on eleven chromosomes and one scaffold, with distinct types and numbers of cis-acting elements in their promoter regions. Whole-genome duplication was the main driving force for the expansion of the MaNF-Y family genes. qRT-PCR analysis indicated that 13 NF-Y genes were involved in regulation of harvested banana fruit ripening. Of the
Acknowledgements
This work was supported by the Natural Science Foundation of China (Nos. 31830070, 31772041 and 31701670), the Science and Technology Planning Project of Guangzhou, China (Nos. 201804020041 and 201604020048), the Science and Technology Planning Project of Guangdong Province, China (No. 2015B090901058). The wok also was supported by Key Laboratory of Plant Resource Conservation and Sustainable Utilization, CAS, China.
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These authors contributed equally to this work.