Glycogen synthase kinases in model and crop plants – From negative regulators of brassinosteroid signaling to multifaceted hubs of various signaling pathways and modulators of plant reproduction and yield

Abstract

Glycogen synthase kinases, also known as SHAGGY-like Kinases (GSKs/SKs), are highly conserved serine/threonine protein kinases present both in animals and plants. Plant genomes contain multiple homologs of the GSK3 genes which participate in various biological processes. Plant GSKs/SKs, and their best known representative in Arabidopsis thaliana – Brassinosteroid Insentisive2 (BIN2/SK21) in particular, were first identified as components of the brassinosteroid (BR) signaling pathway. As phytohormones, BRs regulate a wide range of physiological processes in plants – from germination, cell division, elongation and differentiation to leaf senescence, and response to environmental stresses. The GSKs/SKs proteins belong to a group of several highly conserved components of the BR signaling which evolved early during evolution of this molecular relay. However, recent reports indicated that the GSKs/SKs proteins are also implicated in signaling pathways of other phytohormones and stress-response processes. As a consequence, the GSKs/SKs proteins became hubs of various signaling pathways and modulators of plant development and reproduction. Thus, it is very important to understand molecular mechanisms regulating activity of the GSKs/SKs proteins, but also to get insights into role of the GSKs/SKs proteins in modulation of stability and activity of various substrate proteins which participate in the numerous signaling pathways. Although elucidation of these aspects is still in progress, this review presents a comprehensive and detailed description of these processes and their implications for regulation of development, stress response, and reproduction of model and crop species. The GSKs/SKs proteins and their activity are modulated through phosphorylation and de-phosphorylation reactions which are regulated by various proteins. Importantly, both phosphorylations and de-phosphorylations may have positive and negative effects on the activity of the GSKs/SKs proteins. Additionally, the activity of the GSKs/SKs proteins is positively regulated by reactive oxygen species, whereas it is negatively regulated through ubiquitylation, deacetylation, and nitric oxide-mediated nitrosylation. On the other hand, the GSKs/SKs proteins interact with proteins representing various signaling pathways, and on the basis of the complicated network of interactions the GSKs/SKs proteins differentially regulate various physiological, developmental, stress response, and yield-related processes.

Regulatory network of GSK3-like kinases and their role in plant stress response

“…For example, there are ten and nine GSK3-like kinases in the dicot arabidopsis (Arabidopsis thaliana) and the monocot rice (Oryza sativa), respectively (Qi et al, 2013;Youn and Kim, 2015). The GSK3-like genes have also been identified in several important crop species, such as barley (Hordeum vulgare), cotton (Gossypium hirsutum), maize (Zea mays), pepper (Capsicum annuum), potato (Solanum tuberosum), sorghum (Sorghum bicolor), soybean (Glycine max), wheat (Triticum aestivum) (Table 1) (Chen et al, 2003;Hirano et al, 2017;Qiu et al, 2018;Wang et al, 2018b;Cheng et al, 2020;Kloc et al, 2020;Wang et al, 2020;He et al, 2021;Huang et al, 2021;Wang et al, 2022;Zolkiewicz and Gruszka, 2022;Zhang et al, 2022b). Multiple copies of GSK3 in plant genomes indicate that this gene plays important and diverse roles in the evolutionary adaptation and life strategies of plants (Qi et al, 2013;Li et al, 2021).…”

“…The bin2 bil1 bil2 triple mutants showed a constitutive BR-activation phenotype (Yan et al, 2009). The BR signaling has been well elucidated and proved to be an important regulator of plant physiological and biological processes including seed germination, cell division, elongation and differentiation, leaf senescence and response to biotic and abiotic stresses (Rozhon et al, 2010;Kondo et al, 2014;Dong et al, 2015;Anwar et al, 2018;Peres et al, 2019;Ackerman-Lavert and Savaldi-Goldstein, 2020;Tamaki et al, 2020;Zolkiewicz and Gruszka, 2022). BRs are recognized by the leucine-rich repeat receptor-like (LRR-RLK) protein brassinosteroid-insensitive 1 (BRI1) and its co-receptor BRI1 associated receptor kinase 1 (BAK1) at the membrane (Wang et al, 2008;Santiago et al, 2013).…”

“…GSK3s can phosphorylate a series of substrates including transcription factors, cofactors, kinases, scaffold proteins, cytoskeleton proteins, cyclins, metabolic enzymes, and components of the ubiquitin-proteasome system (UPS). The role of GSK3s in modulating proteins including kinases, scaffold proteins, cytoskeleton proteins, cyclins, metabolic enzymes, and components of the ubiquitin-proteasome system (UPS), has been extensively discussed in several excellent recent reviews (Youn and Kim, 2015;Li et al, 2021;Mao et al, 2021;Zolkiewicz and Gruszka, 2022). In this section, we mainly focus on the discoveries about effects of GSK3s on the transcription factors and cofactors, which play essential roles in modulating stress responsive gene expression.…”

Genome-Wide Association Study and Prediction of Tassel Weight of Tropical Maize Germplasm in Multi-Parent Population

“…Subsequent investigations of the gene structure, phylogeny, and functional regulation of GSK3/SHAGGY-like kinases have intensified because of their pivotal roles in diverse physiological and developmental processes. These processes encompass cell growth, root and stomatal development, inflorescence development, light responses, and stress responses and are achieved through the phosphorylation of multiple substrates [36][37][38][39]. In Arabidopsis thaliana, BRASSINOSTEROID-INSENSITIVE 2 (BIN2) plays a crucial role in steroid signaling regulation.…”

Plant Defense and Viral Counter-Defense during Plant–Geminivirus Interactions

“…Several geminiviral genes, such as C4/AC4, are reported to interact with many Shaggy-like protein kinases [ 97 ]. Shaggy-like protein kinase SKη negatively regulates brassinosteroid (BR) signaling [ 98 ]. C4–SKη interactions are critical for C4 multifunctions, including viral symptom induction, RNA silencing suppression, cell cycle and BR signaling regulation, the induction of hyperplasia and cell division [ 99 , 100 ].…”