WHIRLIES Are Multifunctional DNA-Binding Proteins With Impact on Plant Development and Stress Resistance

Abstract

WHIRLIES are plant-specific proteins binding to DNA in plastids, mitochondria, and nucleus. They have been identified as significant components of nucleoids in the organelles where they regulate the structure of the nucleoids and diverse DNA-associated processes. WHIRLIES also fulfil roles in the nucleus by interacting with telomers and various transcription factors, among them members of the WRKY family. While most plants have two WHIRLY proteins, additional WHIRLY proteins evolved by gene duplication in some dicot families. All WHIRLY proteins share a conserved WHIRLY domain responsible for ssDNA binding. Structural analyses revealed that WHIRLY proteins form tetramers and higher-order complexes upon binding to DNA. An outstanding feature is the parallel localization of WHIRLY proteins in two or three cell compartments. Because they translocate from organelles to the nucleus, WHIRLY proteins are excellent candidates for transducing signals between organelles and nucleus to allow for coordinated activities of the different genomes. Developmental cues and environmental factors control the expression of WHIRLY genes. Mutants and plants with a reduced abundance of WHIRLY proteins gave insight into their multiple functionalities. In chloroplasts, a reduction of the WHIRLY level leads to changes in replication, transcription, RNA processing, and DNA repair. Furthermore, chloroplast development, ribosome formation, and photosynthesis are impaired in monocots. In mitochondria, a low level of WHIRLIES coincides with a reduced number of cristae and a low rate of respiration. The WHIRLY proteins are involved in the plants’ resistance toward abiotic and biotic stress. Plants with low levels of WHIRLIES show reduced responsiveness toward diverse environmental factors, such as light and drought. Consequently, because such plants are impaired in acclimation, they accumulate reactive oxygen species under stress conditions. In contrast, several plant species overexpressing WHIRLIES were shown to have a higher resistance toward stress and pathogen attacks. By their multiple interactions with organelle proteins and nuclear transcription factors maybe a comma can be inserted here? and their participation in organelle–nucleus communication, WHIRLY proteins are proposed to serve plant development and stress resistance by coordinating processes at different levels. It is proposed that the multifunctionality of WHIRLY proteins is linked to the plasticity of land plants that develop and function in a continuously changing environment.

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 .…”

“…Our analysis shows that gene replication plays a major role in gene family expansion. Moreover, both Ka/Ks ratios were less than 0, suggesting that replication of the MsWHY genes occurs through purification selection and that the corresponding MsWHY proteins are considered to be relatively conservative 68 . In addition, the predicted earliest dates of duplication events in the MsWHY genes segmental duplication pairs ranged from 0.438 to 20.051 million years ago, these results suggest that this is an ancient gene family.…”

“…Transcription factors play an important role in regulating plant growth and development 67 . Through the regulation of a transcription factor, it can achieve the regulation of multiple functional related genes, to achieve the purpose of improving plant traits 68 . In this study, bioinformatics methods were used to analyze the transcription factors of alfalfa WHY and provide favorable evidence for the verification of its related functions, which provides a sufficient basis for the cultivation of alfalfa in the future.…”

“…The small family of WHY proteins are single-strand DNA/RNA binding proteins located in organelles and nuclei with a characteristic "whirligig" secondary structure and a conserved KGKAAL DNA binding domain in angiosperms 1 . WHIRLY domains are comprised of four structural topologies that are characterized by two antiparallel four strands of β sheets enabled by a C-terminal helix-loop-helix motif 2 , 3 .…”

“…WHIRLY domains are comprised of four structural topologies that are characterized by two antiparallel four strands of β sheets enabled by a C-terminal helix-loop-helix motif 2 , 3 . Higher plants share a KGKAAL motif in the WHIRLY domain that mediates binding to single-strand DNA (ssDNA) 1 . In addition, WHY-like proteins with a high structural similarity but lacking the KGKAAL motif are also found in green algae 4 .…”