Genome-wide investigation of histone acetyltransferase gene family and its responses to biotic and abiotic stress in foxtail millet (Setaria italica [L.] P. Beauv)

Abstract

Background: Modification of histone acetylation is a ubiquitous and reversible process in eukaryotes and prokaryotes and plays crucial roles in the regulation of gene expression during plant development and stress responses. Histone acetylation is co-regulated by histone acetyltransferase (HAT) and histone deacetylase (HDAC). HAT plays an essential regulatory role in various growth and development processes by modifying the chromatin structure through interactions with other histone modifications and transcription factors in eukaryotic cells, affecting the transcription of genes. Comprehensive analyses of HAT genes have been performed in Arabidopsis thaliana and Oryza sativa. However, little information is available on the HAT genes in foxtail millet (Setaria italica [L.] P. Beauv).

Results: In this study, 24 HAT genes (SiHATs) were identified and divided into four groups with conserved gene structures via motif composition analysis. Phylogenetic analysis of the genes was performed to predict functional similarities between Arabidopsis thaliana, Oryza sativa, and foxtail millet; 19 and 2 orthologous gene pairs were individually identified. Moreover, all identified HAT gene pairs likely underwent purified selection based on their non-synonymous/synonymous nucleotide substitutions. Using published transcriptome data, we found that SiHAT genes were preferentially expressed in some tissues and organs. Stress responses were also examined, and data showed that SiHAT gene transcription was influenced by drought, salt, low nitrogen, and low phosphorus stress, and that the expression of four SiHATs was altered as a result of infection by Sclerospora graminicola.

Conclusions: Results indicated that histone acetylation may play an important role in plant growth and development and stress adaptations. These findings suggest that SiHATs play specific roles in the response to abiotic stress and viral infection. This study lays a foundation for further analysis of the biological functions of SiHATs in foxtail millet.

Keywords: Abiotic stress; Expression analysis; Nitrogen deficiency; Phosphorus deficiency; Sclerospora graminicola infection; SiHAT genes.

Fig. 1

Chromosome locations of histone acetylation genes (HATs) in Setaria italica. Chromosomal location was performed on 24 histone acetylation gene family members in S. italica

Fig. 2

Maximum likelihood phylogenetic trees and structure and conserved domains of histone acetylation gene (HAT) in Setaria italica (Si). a Phylogenetic tree and subfamily of SiHATs, which are further divided into four groups. b The exon-intron organization of SiHATs. c Conserved domain of the HAT protein in foxtail millet. Bromo domains are conserved domain of GNAT subfamily; PHD, ZnF and ZZ are conserved domains of CBP subfamily, and TBP-binding domains are conserved domain of TAF subfamily

Fig. 3

Phylogenetic analysis and Collinearity analysis of histone acetylation proteins (HATs) in Arabidopsis thaliana (At), Oryza sativa (Os), and Setaria italica (Si). a Phylogenetic tree of HAT genes. b Collinearity of foxtail millet HAT and related species. The green rectangular color block represents the foxtail millet chromosome, yellow rectangular color block represents the rice chromosome and red rectangular block represents Arabidopsis chromosome. The number represents the chromosome number

Fig. 4

Maximum likelihood phylogenetic trees and prediction of cis-acting elements in promoter of histone acetylation genes ( HAT s) in Setaria italica (Si). a Phylogenetic trees of foxtail millet HAT genes. b Promoter analysis of foxtail millet HAT genes. The 2 Kb promoter sequences of corresponding HAT genes were used to analyze hormone-related cis-elements, plant growth and development cis-elements and stress-related elements. Different cis-elements were indicated by different colored symbols and placed in their relative position on the promoter of SiHATs

Fig. 5

Relative expression patterns of histone acetylation genes (HATs) in different tissues of Setaria italica. Heat maps reflect the fragments per kilobase of transcript per million mapped fragments (FPKM) of HATs. Color from red to blue indicates high to low expression

Fig. 6

Expression analysis of histone acetylation genes (HATs) in Setaria italica under low nitrogen stress. Low nitrate stress time represented by 10 min, 30 min, 2, 8, 24, and 72 h, NN and LN represent normal and low nitrogen treatment, respectively. Leaf and Root describe tissues sampled

Fig. 7

Expression analysis of histone acetylation genes (HATs) in Setaria italica under low phosphorus stress. Low phosphorus stress time represented by 0.5, 2, 6, 12, 24, and 72 h. NP and LP represent normal and low phosphorus treatments, respectively. Leaf and Root describe tissues sampled

Fig. 8

Expression analysis of HATs genes in foxtail millet under drought stress. Control and Drought represented Control and Drought treatment groups, respectively. R (AN04) and S (Yugu1) represent drought-resistant and drought-sensitive varieties, respectively. Light and Dark represent different sampling times and illumination: (light) illumination, (dark) no illumination

Fig. 9

Expression analysis of HATs genes in foxtail millet under salt-alkali stress. CK and SAS represent control group and salt-alkali treatment group, respectively. R (B103) and S (B355) represent salt-resistant and salt-sensitive varieties, respectively. T1 and T2 represent different sampling tissues: T1 is Seedlings germinating for 3 days and T2 is one-tip-two-leaf Seedlings

Fig. 10

Expression analysis histone acetylation genes (HATs) in Setaria italica under Sclerospora graminicola infection stress. CK and T represent the control and infection treatment groups, respectively. R and S represent resistant and sensitive varieties, respectively. Numbers 3, 5, and 7 represent leaf stages at different sampling times