BACKGROUND: The increasing ambient temperature significantly impacts plant growth, development, and reproduction. Uncovering the temperature-regulating mechanisms in plants is of high importance, for increasing our fundamental understanding of plant thermomorphogenesis, for its potential in applied science, and for aiding plant breeders in improving plant thermoresilience. Thermomorphogenesis, the developmental response to warm temperatures, has been primarily studied in seedlings and in the regulation of flowering time. PHYTOCHROME B and PHYTOCHROME-INTERACTING FACTORs (PIFs), particularly PIF4, are key components of this response. However, the thermoresponse of other adult vegetative tissues and reproductive structures has not been systematically evaluated, especially concerning the involvement of phyB and PIFs. RESULTS: We screened the temperature responses of the wild type and several phyB-PIF4 pathway Arabidopsis mutant lines in combined and integrative phenotyping platforms for root growth in soil, shoot, inflorescence, and seed. Our findings demonstrate that phyB-PIF4 is generally involved in the relay of temperature signals throughout plant development, including the reproductive stage. Furthermore, we identified correlative responses to high ambient temperature between shoot and root tissues. This integrative and automated phenotyping was complemented by monitoring the changes in transcript levels in reproductive organs. Transcriptomic profiling of the pistils from plants grown under high ambient temperature identified key elements that may provide insight into the molecular mechanisms behind temperature-induced reduced fertilization rate. These include a downregulation of auxin metabolism, upregulation of genes involved auxin signalling, miRNA156 and miRNA160 pathways, and pollen tube attractants. CONCLUSIONS: Our findings demonstrate that phyB-PIF4 involvement in the interpretation of temperature signals is pervasive throughout plant development, including processes directly linked to reproduction.

• Keywords
• Arabidopsis, Automatic phenotyping, PIF4, Pistils, Pollen tube guidance, Seeds, Thermomorphogenesis, phyB,
• MeSH
• Arabidopsis * genetics   metabolism   growth & development   physiology   MeSH
• Phenotype * MeSH
• Phytochrome B * metabolism   genetics   MeSH
• Plant Roots genetics   metabolism   growth & development   MeSH
• Flowers genetics   growth & development   MeSH
• Arabidopsis Proteins * genetics   metabolism   MeSH
• Gene Expression Regulation, Plant MeSH
• Signal Transduction MeSH
• Basic Helix-Loop-Helix Transcription Factors * genetics   metabolism   MeSH
• Hot Temperature MeSH
• Publication type
• Journal Article MeSH
• Names of Substances
• Phytochrome B * MeSH
• PHYB protein, Arabidopsis MeSH Browser
• PIF4 protein, Arabidopsis MeSH Browser
• Arabidopsis Proteins * MeSH
• Basic Helix-Loop-Helix Transcription Factors * MeSH

BACKGROUND: Plant sexual reproduction is highly sensitive to elevated ambient temperatures, impacting seed development and production. We previously phenotyped this effect on three rapeseed cultivars (DH12075, Topas DH4079, and Westar). This work describes the transcriptional response associated with the phenotypic changes induced by heat stress during early seed development in Brassica napus. RESULTS: We compared the differential transcriptional response in unfertilized ovules and seeds bearing embryos at 8-cell and globular developmental stages of the three cultivars exposed to high temperatures. We identified that all tissues and cultivars shared a common transcriptional response with the upregulation of genes linked to heat stress, protein folding and binding to heat shock proteins, and the downregulation of cell metabolism. The comparative analysis identified an enrichment for a response to reactive oxygen species (ROS) in the heat-tolerant cultivar Topas, correlating with the phenotypic changes. The highest heat-induced transcriptional response in Topas seeds was detected for genes encoding various peroxidases, temperature-induced lipocalin (TIL1), or protein SAG21/LEA5. On the contrary, the transcriptional response in the two heat-sensitive cultivars, DH12075 and Westar, was characterized by heat-induced cellular damages with the upregulation of genes involved in the photosynthesis and plant hormone signaling pathways. Particularly, the TIFY/JAZ genes involved in jasmonate signaling were induced by stress, specifically in ovules of heat-sensitive cultivars. Using a weighted gene co-expression network analysis (WGCNA), we identified key modules and hub genes involved in the heat stress response in studied tissues of either heat-tolerant or sensitive cultivars. CONCLUSIONS: Our transcriptional analysis complements a previous phenotyping analysis by characterizing the growth response to elevated temperatures during early seed development and reveals the molecular mechanisms underlying the phenotypic response. The results demonstrated that response to ROS, seed photosynthesis, and hormonal regulation might be the critical factors for stress tolerance in oilseed rape.

• Keywords
• Brassica napus, Embryo, Ovule, Seed, Thermomorphogenesis, Transcriptomics,
• MeSH
• Brassica napus * metabolism   MeSH
• Reactive Oxygen Species metabolism   MeSH
• Gene Expression Regulation, Plant MeSH
• Seeds metabolism   MeSH
• Gene Expression Profiling MeSH
• Transcriptome MeSH
• Ovule MeSH
• Publication type
• Journal Article MeSH
• Names of Substances
• Reactive Oxygen Species MeSH