HsfA1a confers pollen thermotolerance through upregulating antioxidant capacity, protein repair, and degradation in Solanum lycopersicum L.

Abstract

The heat shock transcription factors (Hsfs) play critical roles in plant responses to abiotic stresses. However, the mechanism of Hsfs in the regulation of pollen thermotolerance and their specific biological functions and signaling remain unclear. Herein, we demonstrated that HsfA1a played a key role in tomato pollen thermotolerance. hsfA1a mutants reduced, while its overexpression increased pollen themotolerance based on the pollen viability and germination. Analyzing the whole transcriptome by RNA-Seq data, we found that HsfA1a mainly regulated the genes involved in oxidative stress protection, protein homeostasis regulation and protein modification, as well as the response to biological stress in anthers under heat stress. The accumulation of reactive oxygen species in anthers were enhanced in hsfA1a mutants, while were decreased in HsfA1a overexpressing lines. Furthermore, the bounding of HsfA1a to the promoter region of genes involved in redox regulation (Cu/Zn-SOD, GST8 and MDAR1), protein repair (HSP17.6A, HSP70–2, HSP90–2 and HSP101) and degradation (UBP5, UBP18, RPN10a and ATG10) and regulated the expression of these genes in tomato anthers under heat stress. Our findings suggest that HsfA1a maintains pollen thermotolerance and cellular homeostasis by enhancing the antioxidant capacity and protein repair and degradation, ultimately improving pollen viability and fertility.

Crosstalk between endoplasmic reticulum and cytosolic unfolded protein response in tomato

“…This result raised the question whether HsfA1a exerts a transcriptional regulation of ATG genes. We examined the expression of nine ATG genes that are either HS-induced based on an in-house RNAseq (from leaves exposed to 40 vs 25 °C for 1 h; unpublished), or the presence of HSEs and regulation by HsfA1a either under drought or heat stress conditions as shown previously by other groups (Wang et al 2015;Xie et al 2022). We did not detect any significant induction of ATG genes in response to TUN treatment (Fig.…”

“…ER stress induces autophagy as a protective mechanism against the accumulation of toxic protein aggregates . Considering that HS also induces autophagy in an HsfA1a-dependent manner (Xie et al 2022), we examined the formation of autophagosomes in protoplasts isolated from leaves of WT, A1CS, and A1aOE plants using the MDC staining method (Bao et al 2018). We observed a low number of autophagosomes in protoplasts of all genotypes treated with DMSO (Fig.…”

“…Autophagy is also mediated by the activity of HSFs. ATG10 and ATG18f are regulated by tomato HsfA1a in response to drought, and ATG10 in tomato pollen heat stress response (Wang et al 2015;Xie et al 2022).…”

MAPK20-mediated ATG6 phosphorylation is critical for pollen development in Solanum lycopersicum L.

“…The pollen viability and germination in vitro were analysed as described by Xie et al. [ 73 ]. The pollen germination in vivo was measured as previously described [ 11 ].…”

“…MDC staining was performed as the method described by Xie et al. [ 73 ]. For detecting the level of ATG8, the proteins were isolated and immunoblotted as described in a previous study [ 78 ].…”