Genome-wide analysis of histone acetyltransferase and histone deacetylase families and their expression in fruit development and ripening stage of pepper (Capsicum annuum)

Abstract

The fruit development and ripening process involve a series of changes regulated by fine-tune gene expression at the transcriptional level. Acetylation levels of histones on lysine residues are dynamically regulated by histone acetyltransferases (HATs) and histone deacetylases (HDACs), which play an essential role in the control of gene expression. However, their role in regulating fruit development and ripening process, especially in pepper (Capsicum annuum), a typical non-climacteric fruit, remains to understand. Herein, we performed genome-wide analyses of the HDAC and HAT family in the pepper, including phylogenetic analysis, gene structure, encoding protein conserved domain, and expression assays. A total of 30 HAT and 15 HDAC were identified from the pepper genome and the number of gene differentiation among species. The sequence and phylogenetic analysis of CaHDACs and CaHATs compared with other plant HDAC and HAT proteins revealed gene conserved and potential genus-specialized genes. Furthermore, fruit developmental trajectory expression profiles showed that CaHDAC and CaHAT genes were differentially expressed, suggesting that some are functionally divergent. The integrative analysis allowed us to propose CaHDAC and CaHAT candidates to be regulating fruit development and ripening-related phytohormone metabolism and signaling, which also accompanied capsaicinoid and carotenoid biosynthesis. This study provides new insights into the role of histone modification mediate development and ripening in non-climacteric fruits.

Genome-wide identification, phylogenetic classification of histone acetyltransferase genes, and their expression analysis in sugar beet (Beta vulgaris L.) under salt stress

“…Four histone acetyltransferase families including GNAT (GCN5, ELP3 and HAT1), MYST (HAG4 and HAG5), p300/CBP (HAC1, HAC2, HAC4, HAC5, and HAC12) and TAFII250 (HAF1 and HAF2) are present in Arabidopsis genome (Pandey et al 2002 ). A total of 12, 8, 32, 7, 6, 31, 14, 24, and 30 HAT-encoding genes were characterized in different plant species, such as Arabidopsis (Pandey et al 2002 ), Oryza sativa (rice) (Liu et al 2012 ), Solanum lycopersicum (tomato) (Aiese Cigliano et al 2013 ; Hawar et al 2021 ), Vitis vinifera (grapevine) (Aquea et al 2010 ), Litchi chinensis (litchi) (Peng et al 2017 ), Triticum aestivum (wheat) (Gao et al 2021 ), Citrus sinensis (citrus) (Shu et al 2021 ), Setaria italica (foxtail millet) (Xing et al 2022 ), and Capsicum annuum (pepper) (Cai et al 2022 ), respectively. HATs were reported to be involved in development, root stem cell niche maintenance, fruit development, flowering, and abiotic/biotic stress response in plants (Gao et al 2021 ; Cai et al 2022 ).…”

“…A total of 12, 8, 32, 7, 6, 31, 14, 24, and 30 HAT-encoding genes were characterized in different plant species, such as Arabidopsis (Pandey et al 2002 ), Oryza sativa (rice) (Liu et al 2012 ), Solanum lycopersicum (tomato) (Aiese Cigliano et al 2013 ; Hawar et al 2021 ), Vitis vinifera (grapevine) (Aquea et al 2010 ), Litchi chinensis (litchi) (Peng et al 2017 ), Triticum aestivum (wheat) (Gao et al 2021 ), Citrus sinensis (citrus) (Shu et al 2021 ), Setaria italica (foxtail millet) (Xing et al 2022 ), and Capsicum annuum (pepper) (Cai et al 2022 ), respectively. HATs were reported to be involved in development, root stem cell niche maintenance, fruit development, flowering, and abiotic/biotic stress response in plants (Gao et al 2021 ; Cai et al 2022 ). Two MYST genes, HAM1 and HAM2 in Arabidopsis are functionally redundant gene pairs, Arabidopsis ham1 ham2 double mutants showed severe defects in the male and female gametophyte development (Latrasse et al 2008 ).…”

“…Less is known about the involvement of epigenetic alterations on plant metabolism and physiology when compared to mammals. Genome-wide studies were performed to discover HAT genes in crop species, and their expression profiles varied in different tissues, developmental stages, and according to type and duration of stress (Cai et al 2022 ; Shu et al 2021 ; Xing et al 2022 ; Gao et al 2021 ; Peng et al 2017 ). For example, HAT genes in Setaria italica were found to respond to different stresses, such as salt, drought, low nitrogen, and low phosphorus (Xing et al 2022 ).…”

“…For example, HAT genes in Setaria italica were found to respond to different stresses, such as salt, drought, low nitrogen, and low phosphorus (Xing et al 2022 ). The transcription abundances of Capsicum annuum HATs (CaHAM1, CaHAG7, CaHA14, CaHAG5, and CaHAC4) were upregulated at the early development stages of fruits, while the others were transcribed at the late developmental stages, suggesting the involvement of HATs in the regulation of fruit ripening (Cai et al 2022 ). In a recent study, drought stress led to increase the expression of Citrus sinensis HAT genes (CsHAT6, 13, and 14) , and decrease CsHAT5 and CsHAT8 transcription levels (Shu et al 2021 ).…”

ZmELP1, an Elongator complex subunit, is required for the maintenance of histone acetylation and RNA Pol II phosphorylation in maize kernels

“…HATs transfer an acetyl group onto the specific lysine (K) residues at the N‐terminal tails of histones, and this transfer usually weakens the binding of histones to DNA and relaxes the chromatin structure, which lead to transcriptional activation (Struhl, 1998 ; Verdin and Ott, 2015 ). Based on sequence characterization, plant HATs can be grouped into four families: cAMP‐responsive element binding protein (CREB)‐binding proteins (p300/CBPs); TATA‐binding protein‐associated factors (TAFII250s); MOZ, Ybf2/Sas3, Sas2 and Tip60s (MYSTs); general control non‐depressible 5 (GCN5)‐related acetyltransferases (GNATs) (Cai et al ., 2022 ; Hu et al ., 2019 ; Wang et al ., 2014 ). In Arabidopsis, the nucleosomal acetyltransferase of H4 (NuA4) complex stimulates the expression of growth‐ and photosynthesis‐related genes and is needed for chlorophyll biosynthesis and the stress response (Bieluszewski et al ., 2022 ; Zhou et al ., 2022 ).…”