Warm temperature perceived at the vegetative stage affects progeny seed germination in natural accessions of Arabidopsis thaliana

• Published in: The New phytologist 2025-01, Vol.245 (2), p.668-683
• Main Authors: Wang, Yu, Zhang, Tania L., Barnett, Emma M., Sureshkumar, Sridevi, Balasubramanian, Sureshkumar, Fournier‐Level, Alexandre
• Format: Article
• Language: English
• Subjects: Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - physiology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; climate change; dormancy; Ecotype; Endosperm; Exposure; Gene expression; Gene Expression Regulation, Plant; Genetic analysis; Genetic control; Genome-Wide Association Study; Genomes; Genomic analysis; Genotype; Genotypes; Germination; Germination - genetics; Germination - radiation effects; High temperature; Life cycle; maternal effect; Natural populations; Offspring; PHYB; Phytochrome B - genetics; Phytochrome B - metabolism; Plant Leaves - genetics; Plant Leaves - growth & development; Plant Leaves - physiology; Plant Leaves - radiation effects; Plants (botany); Population genetics; Progeny; Seed germination; Seeds; Seeds - genetics; Seeds - growth & development; Seeds - physiology; Temperature; transgenerational effect
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.20241

Summary Temperatures perceived early in the life cycle of mother plants can affect the germination of the offspring seeds. In Arabidopsis thaliana, vernalisation‐insensitive mutants showed altered germination response to elevated maternal temperature, hence revealing a strong genetic determinism. However, the genetic control of this maternal effect and its prevalence across natural populations remain unclear. Here, we exposed a collection of European accessions of A. thaliana to increased temperature during the vegetative phase and assessed germination in their progeny to identify the genetic basis of transgenerational germination response. We found that genotypes with rapidly germinating progeny after early maternal exposure to elevated temperature originated from regions with low‐light radiation. Combining genome‐wide association, expression analysis and functional assays across multiple genetic backgrounds, we show a central role for PHYB in mediating the response to maternally perceived temperature at the vegetative stage. Differential gene expression analysis in leaves identified a similar genetic network as previously found in seed endosperm under elevated temperature, supporting the pleiotropic involvement of PHYB signalling across different tissues and stages. This provides evidence that complex environmental responses modulated by the maternal genotype can rely on a consistent set of genes yet produce different effects at the different stages of exposure.