A conserved HSF:miR169:NF‐YA loop involved in tomato and Arabidopsis heat stress tolerance

Abstract

Heat stress transcription factors (HSFs) and microRNAs (miRNAs) regulate different stress and developmental networks in plants. Regulatory feedback mechanisms are at the basis of these networks. Here, we report that plants improve their heat stress tolerance through HSF-mediated transcriptional regulation of MIR169 and post-transcriptional regulation of Nuclear Factor-YA (NF-YA) transcription factors. We show that HSFs recognize tomato (Solanum lycopersicum) and Arabidopsis MIR169 promoters using yeast one-hybrid/ chromatin immunoprecipitation-quantitative PCR. Silencing tomato HSFs using virus-induced gene silencing (VIGS) reduced Sly-MIR169 levels and enhanced Sly-NF-YA9/A10 target expression. Further, Sly-NF-YA9/A10 VIGS knockdown tomato plants and Arabidopsis plants overexpressing At-MIR169d or At-nf-ya2 mutants showed a link with increased heat tolerance. In contrast, Arabidopsis plants overexpressing At-NF-YA2 and those expressing a non-cleavable At-NF-YA2 form (miR169d-resistant At-NF-YA2) as well as plants in which At-miR169d regulation is inhibited (miR169d mimic plants) were more sensitive to heat stress, highlighting NF-YA as a negative regulator of heat tolerance. Furthermore, post-transcriptional cleavage of NF-YA by elevated miR169 levels resulted in alleviation of the repression of the heat stress effector HSFA7 in tomato and Arabidopsis, revealing a retroactive control of HSFs by the miR169:NF-YA node. Hence, a regulatory feedback loop involving HSFs, miR169s and NF-YAs plays a critical role in the regulation of the heat stress response in tomato and Arabidopsis plants.

Tomato plant response to heat stress: a focus on candidate genes for yield-related traits

“…Lastly, circRNAs are a class of endogenous ncRNAs characterized by covalently closed structures without 5′ or 3′ ends ( Bhogireddy et al., 2021 ). Rao et al. (2022b) investigated the tomato response to HS and they reported that plants improve their HS tolerance through Hsf-mediated transcriptional regulation of miR169s.…”

“…Lastly, circRNAs are a class of endogenous ncRNAs characterized by covalently closed structures without 5′ or 3′ ends (Bhogireddy et al, 2021). Rao et al (2022b) investigated the tomato response to HS and they reported that plants improve their HS tolerance through Hsfmediated transcriptional regulation of miR169s. HsfA1a, HsfA2 and HsfA7a have a key role in HS response and they also bind to the promoters of miR169, leading to transcriptional enhancement of miR169s.…”

miRNAs and lncRNAs in tomato: Roles in biotic and abiotic stress responses

“…Low temperature will down-regulate the expression of miR164a/b-5p, release the inhibition of NAM3, and improve the cold tolerance of tomato ( Dong et al., 2022 ). High temperature upregulates the expression of miR319d and miR169, and inhibiting the transcription of downstream target genes to improve tomato heat tolerance ( Shi et al., 2019 ; Rao et al., 2022 ). However, the target genes of miR319d at high temperature are unknown.…”

“…Besides this miRNA, miR169 also appears to be involved in heat tolerance regulatory network in tomato. Over-expression of miR169 can significantly inhibit the expression of its target gene NF-YA9/10, and result in the markedly increased activity of its downstream ascorbate peroxidase (APX) (H 2 O 2 scavenging enzyme), then improved tomato heat tolerance ( Rao et al., 2020 ; Rao et al., 2022 ). In addition, miR167a acts as a responsive medium under a variety of abiotic stresses.…”

Advances in the Study of the Transcriptional Regulation Mechanism of Plant miRNAs

“…In recent years, the regulation mechanism of miRNAs in the abiotic response has been discovered in some plants. In Arabidopsis and tomato, the HSF transcription factor is involved in heat stress tolerance through binding to the MIR169 promoter to positively regulate the transcription of MIR169 and negatively regulate the expression of its target gene NF-YA9/10 [ 61 ]. The SERRATE protein, a conserved RNA processing factor in eukaryotes, encodes a C2H2 zinc finger protein.…”