WHIRLY proteins maintain seed longevity by effects on seed oxygen signalling during imbibition

Abstract

The WHIRLY (WHY) family of DNA/RNA binding proteins fulfill multiple but poorly characterized functions in plants. We analysed WHY protein functions in the Arabidopsis Atwhy1,Atwhy3, Atwhy1why3 single and double mutants and wild type controls. The Atwhy3 and Atwhy1why3 double mutants showed a significant delay in flowering, having more siliques per plant but with fewer seeds per silique than the wild type. While germination was similar in the un-aged high-quality seeds of all lines, significant decreases in vigour and viability were observed in the aged mutant seeds compared to the wild type. Imbibition of un-aged high-quality seeds was characterized by large increases in transcripts that encode proteins involved in oxygen sensing and responses to hypoxia. Seed ageing resulted in a disruption of the imbibition-induced transcriptome profile such that transcripts encoding RNA metabolism and processing became the most abundant components of the imbibition signature. The imbibition-related profile of the Atwhy1why3 mutant seeds, was characterised by decreased expression of hypoxia-related and oxygen metabolism genes even in the absence of ageing. Seed ageing further decreased the abundance of hypoxia-related and oxygen metabolism transcripts relative to the wildtype. These findings suggest that the WHY1 and WHY3 proteins regulate the imbibition-induced responses to oxygen availability and hypoxia. Loss of WHY1 and WHY3 functions decreases the ability of Arabidopsis seeds to resist the adverse effects of seed ageing.

Seed longevity and genome damage

“…Changes in transcript levels include components of the translation machinery, as observed in pea seeds subjected to ageing treatments [ 90 ]. Imbibition of aged Arabidopsis seeds leads to large scale transcriptional changes that significantly differ to unaged, high quality seeds [ 91 ]. Imbibed aged Arabidopsis seeds displayed stress responses associated with heat shock and increased expression of genes involved in RNA metabolism [ 91 ].…”

“…Imbibition of aged Arabidopsis seeds leads to large scale transcriptional changes that significantly differ to unaged, high quality seeds [ 91 ]. Imbibed aged Arabidopsis seeds displayed stress responses associated with heat shock and increased expression of genes involved in RNA metabolism [ 91 ]. Consistent with these findings, long-lived Arabidopsis ecotypes display elevated transcript levels of heat shock factors and RNA processing genes, with the corresponding mutant lines displaying altered sensitivity to ageing [ 41 ].…”

Seed Longevity and Ageing: A Review on Physiological and Genetic Factors with an Emphasis on Hormonal Regulation

“…Regarding the biochemical ageing mechanisms, seed deterioration is related to the accumulation of DNA damage, and recent findings point to the WHIRLY (WHY) family of DNA-binding proteins as important players in the maintenance of nuclear and organellar genomes. Longevity of why1 and why3 Arabidopsis mutants was lower than the wild type after wet ageing, and the double mutant why1why3 was highly sensitive to ageing [ 182 ]. In addition, seeds of the why1 mutants are insensitive to the phytohormones ABA and salicylic acid during germination [ 183 ].…”

Plant adaptation to climate change

“…Taylor et al [ 5 ] dedicated their contribution to this themed collection to studying the role of the WHIRLY (WHY) family of DNA/RNA binding proteins. Compared with wild-type controls, germination was similar in unaged high-quality seeds of single and double mutants, but significant decreases in vigor and viability (defined as the ability to germinate, i.e.…”