Role of GhHDA5 in H3K9 deacetylation and fiber initiation in Gossypium hirsutum

Abstract

Cotton fibers are single-celled trichomes that initiate from the epidermal cells of the ovules at or before anthesis. Here, we identified that the histone deacetylase (HDAC) activity is essential for proper cotton fiber initiation. We further identified 15 HDACs homoeologs in each of the A- and D-subgenomes of Gossypium hirsutum. Few of these HDAC homoeologs expressed preferentially during the early stages of fiber development [-1, 0 and 6 days post-anthesis (DPA)]. Among them, GhHDA5 expressed significantly at the time of fiber initiation (-1 and 0 DPA). The in vitro assay for HDAC activity indicated that GhHDA5 primarily deacetylates H3K9 acetylation marks. Moreover, the reduced expression of GhHDA5 also suppresses fiber initiation and lint yield in the RNA interference (RNAi) lines. The 0 DPA ovules of GhHDA5RNAi lines also showed alterations in reactive oxygen species homeostasis and elevated autophagic cell death in the developing fibers. The differentially expressed genes (DEGs) identified through RNA-seq of RNAi line (DEP12) and their pathway analysis showed that GhHDA5 modulates expression of many stress and development-related genes involved in fiber development. The reduced expression of GhHDA5 in the RNAi lines also resulted in H3K9 hyper-acetylation on the promoter region of few DEGs assessed by chromatin immunoprecipitation assay. The positively co-expressed genes with GhHDA5 showed cumulative higher expression during fiber initiation, and gene ontology annotation suggests their involvement in fiber development. Furthermore, the predicted protein interaction network in the positively co-expressed genes indicates HDA5 modulates fiber initiation-specific gene expression through a complex involving reported repressors.

Genome-wide identification and expression patterns analysis of the RPD3/HDA1 gene family in cotton

“…Within the superfamily of HDACs, the RPD3 gene family is the most studied and is crucial in plant development and physiological processes, including flowering time, abiotic stress response, female gametophyte and embryo development, senescence, seed germination, and plant hormone signal response [12-14, 19, 26-28]. To date, although a few studies have analyzed the function of the RPD3 family members in G. hirsutum, they focus primarily on the roles of GhHDA5 in fiber initiation, and there are no systematic reports [29]. To explore the characteristics of RPD3 family members and understand the roles played by cotton RPD3 genes in cotton growth and development, we conducted an integrated analysis of the RPD3 gene family in cotton, containing their phylogenetic relationships, exon-intron structures, conserved motifs, chromosomal distributions, duplication events, expression patterns in different tissues and in the presence of abiotic stresses or MeJA and ABA treatment.…”

“…In short days, AtHDA9 represses the flowering-promoting gene AGL19 (AGAMOUS-LIKE 19) regulated by photoperiod [35] and the downregulation of AtHDA19 causes delayed flowering, flower abnormalities, embryonic defects, and seed set reduction [36]. In recent studies, GhHDA5, similar to AtHDA5 in Arabidopsis, exhibited higher expression at − 1 and 0 DPA, and RNAirepressed GhHDA5 lines showed delayed flowering, suggesting that it may be involved in cotton fiber initiation and flowering time [29]. As the homologous genes of these four AtRPD3 genes related to flowering time in cotton, the gene pairs GhHDA2/GhHDA13, homologous to AtHDA6, and GhHDA6/GhHDA15, homologous to AtHDA9, showed markedly higher expression in earlymaturity cotton compare with late-maturity cotton during all five stages of flower bud differentiation.…”

Updates on molecular mechanisms in the development of branched trichome in Arabidopsis and nonbranched in cotton

“…GhHDA5 RNAi lines changed the ROS homeostasis and elevated autophagic cell death, which, in turn, decreased fibre initiation and lint yield. ChIP‐PCR showed that H3K9 acetylation level on some associated downstream genes regulated by GhHDA5 was up‐regulated in the RNAi lines (Kumar et al ., ). HISTONE MONOUBIQUITINATION2 (HUB2) encoding histone H2B monoubiquitination E3 ligase was shown to have a role in fibre elongation and SCW deposition in transgenic cotton.…”

Genome-wide identification and expression patterns analysis of the RPD3/HDA1 gene family in cotton

“…Within the superfamily of HDACs, the RPD3 gene family is the most studied and is crucial in plant development and physiological processes, including owering time, abiotic stress response, female gametophyte and embryo development, senescence, seed germination, and plant hormone signal response [12-14, 19, 26-28]. To date, although a few studies have analyzed the function of the RPD3 family members in G. hirsutum, they focus primarily on the roles of GhHDA5 in ber initiation, and there are no systematic reports [29]. To explore the characteristics of RPD3 family members and understand the roles played by cotton RPD3 genes in cotton growth and development, we conducted an integrated analysis of the RPD3 gene family in cotton, containing their phylogenetic relationships, exon-intron structures, conserved motifs, chromosomal distributions, duplication events, expression patterns in different tissues and in the presence of abiotic stresses or MeJA and ABA treatment.…”

“…In short days, AtHDA9 represses the owering-promoting gene AGL19 (AGAMOUS-LIKE 19) regulated by photoperiod [35] and the downregulation of AtHDA19 causes delayed owering, ower abnormalities, embryonic defects, and seed set reduction [36]. In recent studies, GhHDA5, similar to AtHDA5 in Arabidopsis, exhibited higher expression at -1 and 0 DPA, and RNAi-repressed GhHDA5 lines showed delayed owering, suggesting that it may be involved in cotton ber initiation and owering time [29]. As the homologous genes of these four AtRPD3 genes related to owering time in cotton, the gene pairs GhHDA2/GhHDA13, homologous to AtHDA6, and GhHDA6/GhHDA15, homologous to AtHDA9, showed markedly higher expression in early-maturity cotton compare with late-maturity cotton during all ve stages of ower bud differentiation.…”