WHIRLY protein functions in plants

Abstract

Environmental stresses pose a significant threat to food security. Understanding the function of proteins that regulate plant responses to biotic and abiotic stresses is therefore pivotal in developing strategies for crop improvement. The WHIRLY (WHY) family of DNA‐binding proteins are important in this regard because they fulfil a portfolio of important functions in organelles and nuclei. The WHY1 and WHY2 proteins function as transcription factors in the nucleus regulating phytohormone synthesis and associated growth and stress responses, as well as fulfilling crucial roles in DNA and RNA metabolism in plastids and mitochondria. WHY1, WHY2 (and WHY3 proteins in Arabidopsis) maintain organelle genome stability and serve as auxiliary factors for homologous recombination and double‐strand break repair. Our understanding of WHY protein functions has greatly increased in recent years, as has our knowledge of the flexibility of their localization and overlap of functions but there is no review of the topic in the literature. Our aim in this review was therefore to provide a comprehensive overview of the topic, discussing WHY protein functions in nuclei and organelles and highlighting roles in plant development and stress responses. In particular, we consider areas of uncertainty such as the flexible localization of WHY proteins in terms of retrograde signalling connecting mitochondria, plastids, and the nucleus. Moreover, we identify WHY proteins as important targets in plant breeding programmes designed to increase stress tolerance and the sustainability of crop yield in a changing climate.

WHIRLY1 Acts Upstream of ABA-Related Reprogramming of Drought-Induced Gene Expression in Barley and Affects Stress-Related Histone Modifications

“…WHIRLIES are a family of small, plant-specific proteins, which intriguingly are localized to endosymbiotic organelles and the nucleus [ 16 , 17 ]. They are discussed to operate as a retrograde signal, and the transfer of WHIRLY1 from the chloroplast to the nucleus has been shown [ 25 ].…”

“…Especially, ABA-signaling pathways have been shown to involve histone-modifying enzymes, e.g., histone deacetylases (HDAs) [ 4 , 13 , 14 , 15 ]. Recently, a plant-specific single-stranded DNA (ss-DNA)-binding protein family called WHIRLY and dually located in plastids or mitochondria and the nucleus has been described [ 16 , 17 ]. This multifunctional protein family, which has denominated WHIRLY due to its protein structure, is involved in plant development and plants’ responses to biotic and abiotic stress [ 14 , 18 , 19 , 20 , 21 , 22 , 23 ].…”

Genome-wide identification, phylogenetic, and expression analysis under abiotic stress conditions of Whirly (WHY) gene family in Medicago sativa L.

“…Members of the WHY protein family are found throughout the plant world, and WHY proteins play several important roles in plant development and stress tolerance. In particular, WHY1 regulates gene expression that encodes numerous housekeeping proteins and regulates plant development in response to biological and abiotic stress 1 , 5 . First, it acts as a transcription factor in the nucleus, regulating the expression of hormones such as ABA and SA, then as an organoid in organelle chloroplasts and mitochondria 5 .…”

“…In particular, WHY1 regulates gene expression that encodes numerous housekeeping proteins and regulates plant development in response to biological and abiotic stress 1 , 5 . First, it acts as a transcription factor in the nucleus, regulating the expression of hormones such as ABA and SA, then as an organoid in organelle chloroplasts and mitochondria 5 . Barley WHY1 deficient plants showed delayed greening and delayed photosynthesis, suggesting WHY1 is necessary for chloroplast biogenesis 16 , 18 .…”

“…In addition, WHY-like proteins with a high structural similarity but lacking the KGKAAL motif are also found in green algae 4 . Although algae have only one similar WHY protein, most plants in nature have two types of WHY proteins, WHY1 and WHY2 5 . WHY1 is a nuclear-localized protein that also targets chloroplasts 6 .…”