The Role of Selective Protein Degradation in the Regulation of Iron and Sulfur Homeostasis in Plants

Abstract

Plants are able to synthesize all essential metabolites from minerals, water, and light to complete their life cycle. This plasticity comes at a high energy cost, and therefore, plants need to tightly allocate resources in order to control their economy. Being sessile, plants can only adapt to fluctuating environmental conditions, relying on quality control mechanisms. The remodeling of cellular components plays a crucial role, not only in response to stress, but also in normal plant development. Dynamic protein turnover is ensured through regulated protein synthesis and degradation processes. To effectively target a wide range of proteins for degradation, plants utilize two mechanistically-distinct, but largely complementary systems: the 26S proteasome and the autophagy. As both proteasomaland autophagy-mediated protein degradation use ubiquitin as an essential signal of substrate recognition, they share ubiquitin conjugation machinery and downstream ubiquitin recognition modules. Recent progress has been made in understanding the cellular homeostasis of iron and sulfur metabolisms individually, and growing evidence indicates that complex crosstalk exists between iron and sulfur networks. In this review, we highlight the latest publications elucidating the role of selective protein degradation in the control of iron and sulfur metabolism during plant development, as well as environmental stresses. are present at certain concentrations, i.e., when the demand meets the supply. Below such levels, the demand for a nutrient exceeds the supply, so plant growth is ultimately limited by a nutritional deficiency. Conversely, an excess of any nutrient is toxic to plants and also negatively affects plant growth and development. Plants can therefore experience transitions between deficiency or toxicity zones due to changes in the availability of nutrients and growth requirements, but they can return to homeostasis so long as the response is adequate and sufficient. Such adjustments may require time, but they are crucial for plant adaptation. A significant part of this adaptation relies on selective protein degradation (Figure 1). Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 21 nutrients are present at certain concentrations, i.e., when the demand meets the supply. Below such levels, the demand for a nutrient exceeds the supply, so plant growth is ultimately limited by a nutritional deficiency. Conversely, an excess of any nutrient is toxic to plants and also negatively affects plant growth and development. Plants can therefore experience transitions between deficiency or toxicity zones due to changes in the availability of nutrients and growth requirements, but they can return to homeostasis so long as the response is adequate and sufficient. Such adjustments may require time, but they are crucial for plant adaptation. A significant part of this adaptation relies on selective protein degradation ( Figure 1). Figure 1.Regulation of nutrient deficiency stress by ubiquitination. The plant perceives nutrient deficienc...

Interaction Between Sulfur and Iron in Plants

“…Identifying a suitable approach to unravel the mechanism underling the Fe/S interplay still remains challenging. The complex regulation of both Fe and S homeostasis involves different regulating pathways with likely different signal molecules ( Wawrzyñska and Sirko, 2020 ). Such complexity relies mainly on the following aspects: (i) different regulating mechanisms might act at local (cell and/or tissue) and systemic level (shoot-root communication); and (ii) nutrient deficiency-induced responses of plants are tailored on the harshness degree of stress.…”

Ferroptosis in plants: triggers, proposed mechanisms, and the role of iron in modulating cell death

“…Furthermore, it was observed that suppressing ironsulfur clusters biosynthesis induces ferroptosis in lung tumors (Alvarez et al, 2017). Interestingly, most of the plant metabolically-active iron is included in these clusters and the selective protein degradation that takes place during abiotic stresses was shown to have an impact on iron metabolism (Wawrzyńska and Sirko, 2020).…”

Influence of Ethylene Signaling in the Crosstalk Between Fe, S, and P Deficiency Responses in Arabidopsis thaliana

“…In relation to Fe deficiency, the master TF is FIT, a bHLH TF which interacts with other related bHLH TFs, like bHLH38 and bHLH39, to activate the expression of Fe starvation genes, like FRO2 and IRT1 (Kobayashi and Nishizawa, 2012 ; Lucena et al, 2015 ; Gao et al, 2019 ; Schwarz and Bauer, 2020 ). Finally, in relation to S deficiency, the master TF is SLIM1, an ethylene insensitive 3-like (EIL3) family TF which could interact with other TFs to activate the expression of S starvation genes, like SULTR1;1 and SULTR1;2 (Maruyama-Nakashita et al, 2006 ; Takahashi et al, 2011 ; Wawrzynska et al, 2015 ; Wawrzynska and Sirko, 2016 , 2020 ; Yamaguchi et al, 2020 ). These master TFs could be regulated transcriptionally and post-transcriptionally.…”

“…Finally, in relation to S nutrition, several S-responsive genes, like SULTR1;1 , are upregulated by S limitation more significantly in wild-type (WT) Arabidopsis than in slim1 mutants (Maruyama-Nakashita et al, 2006 ). SLIM1 was identified as an allele of EIL3 (see above; Maruyama-Nakashita et al, 2006 ), possibly related to ET signaling (Wawrzynska et al, 2015 ; Wawrzynska and Sirko, 2016 , 2020 ).…”