Transcriptome profiling reveals histone deacetylase 1 gene overexpression improves flavonoid, isoflavonoid, and phenylpropanoid metabolism in Arachis hypogaea hairy roots

Abstract

Background The peanut (Arachis hypogaea) is a crop plant of high economic importance, but the epigenetic regulation of its root growth and development has not received sufficient attention. Research on Arabidopsis thaliana has shown that histone deacetylases (HDACs) are involved in cell growth, cell differentiation, and stress response. Few studies have focused on the role of HDACs in the root development of other plants, particularly crop plants. In earlier studies, we found large accumulations of A. hypogaea histone deacetylase 1 (AhHDA1) mRNA in peanut roots. However, we did not explore the role of AhHDA1 in peanut root development. Methods In this paper, we investigated the role of the peanut AhHDA1 gene and focused on the effect of altered AhHDA1 expression in hairy roots at both the phenotypic and transcriptional levels. We analyzed the transformation of A. hypogaea hairy roots using Agrobacterium rhizogenes and RNA sequencing to identify differentially expressed genes that were assigned to specific metabolic pathways. Transgenic hairy roots were used as experimental material to analyze the downstream genes expression and histone acetylation levels. To thoroughly understand AhHDA1 function, we also simultaneously screened the AhHDA1-interacting proteins using a yeast two-hybrid system. Results AhHDA1-overexpressing hairy roots were growth-retarded after 20 d in vitro cultivation, and they had a greater accumulation of superoxide anions and hydrogen peroxide than the control and RNAi groups. AhHDA1 overexpression in hairy roots accelerated flux through various secondary synthetic metabolic pathways, as well as inhibited the primary metabolism process. AhHDA1 overexpression also caused a significant upregulation of genes encoding the critical enzyme chalcone synthase (Araip.B8TJ0, CHS) in the flavonoid biosynthesis pathway, hydroxyisoflavanone synthase (Araip.0P3RJ) in the isoflavonoid biosynthesis pathway, and caffeoyl-CoA O-methyltransferase (Aradu.M62BY, CCoAOMT) in the phenylpropanoid biosynthesis pathway. In contrast, ferredoxin 1 (Araip.327XS), the polypeptide of the oxygen-evolving complex of photosystem II (Araip.N6ZTJ), and ribulose bisphosphate carboxylase (Aradu.5IY98) in the photosynthetic pathway were significantly downregulated by AhHDA1 overexpression. The expression levels of these genes had a positive correlation with histone acetylation levels. Conclusion Our results revealed that the relationship between altered gene metabolism activities and AhHDA1 overexpression was mainly reflected in flavonoid, isoflavonoid, and phenylpropanoid metabolism. AhHDA1 overexpression retarded the growth of transgenic hairy roots and may be associated with cell metabolism status. Future studies should focus on the function of AhHDA1-interacting proteins and their effect on root development.

Biosynthesis and metabolic engineering of isoflavonoids in model plants and crops: a review

“…The biosynthesis of isoflavonoids in plants is intricately regulated by diverse environmental factors (such as UV radiation, fungal infection, nitrogen, and phosphorus deficiencies), through transcriptional regulation, post-translational modifications, and epigenetic changes ( Dastmalchi et al., 2017 ; Su et al., 2021 ; Wang et al., 2023a ).…”

Transcriptomic–Proteomic Analysis Revealed the Regulatory Mechanism of Peanut in Response to Fusarium oxysporum

“…In particular, combined multi-omics analytical methods are widely used in the study of plant–microbial interactions [ 18 , 19 ]. In terms of the functional research related to peanuts, transcriptome and proteome sequencing were used to assist in screening the key genes involved in aerial and subterranean pods [ 20 ], drought resistance [ 21 , 22 ], development [ 23 , 24 ], environmental stress [ 25 ], and interaction with Aspergillus flavus [ 26 ]. In this study, peanut stems infected with F. oxysporum were used as experimental materials.…”

Histone Deacetylase GiSRT2 Negatively Regulates Flavonoid Biosynthesis in Glycyrrhiza inflata

“…For instance, silencing SlHDT3 in tomato decreased carotenoid accumulation [12]. In Arachis hypogaea hairy roots, overexpression of AhHDA1 promotes the accumulation of flavonoids [13]. Treatment of HDAC inhibitors increases the content of ginsenoside in ginseng adventitious roots by cooperating with MeJA [14].…”