The Ubiquitin Proteasome System and Nutrient Stress Response

Abstract

Plants utilize different molecular mechanisms, including the Ubiquitin Proteasome System (UPS) that facilitates changes to the proteome, to mitigate the impact of abiotic stresses on growth and development. The UPS encompasses the ubiquitination of selected substrates followed by the proteasomal degradation of the modified proteins. Ubiquitin ligases, or E3s, are central to the UPS as they govern specificity and facilitate the attachment of one or more ubiquitin molecules to the substrate protein. From recent studies, the UPS has emerged as an important regulator of the uptake and translocation of essential macronutrients and micronutrients. In this review, we discuss select E3s that are involved in regulating nutrient uptake and responses to stress conditions, including limited or excess levels of nitrogen, phosphorus, iron, and copper.

Keywords: 26S proteasome; abiotic stress; nutrient stress; nutrient uptake; protein degradation; ubiquitin ligase; ubiquitination.

Figure 1

(A) A simplified outline of the ubiquitin proteasome system. The E1, E2, and E3 enzymes facilitate attachment of one or more ubiquitin (Ub) molecules to the target substate. Ubiquitination of the target occurs through transfer of Ub from the E2 to the E3 active cysteine prior to attachment to the substrate (i) or direct transfer of Ub to the substrate (ii). The conjugation cascade results in the monoubiquitination (one Ub at one site), multi-monoubiquitination (multiple Ubs at different sites), or polyubiquitination (multiple Ubs forming a chain) of the substrate. Polyubiquitinated substrates are recognized and degraded by the 26S proteasome. Ub is removed from the substrate and recycled. (B) Schematics representation of different E3 types. E3s utilize a RING (Really Interesting New gene), HECT (Homologous to E6AP C-terminus), or U-box domain to interact with the E2. Single subunit HECT and RING-in-between-RING (RBR) type E3s accept the Ub from the E2. Complex E3 Cullin (Cul)-RING ubiquitin ligases (CRLs) utilize different subunits to interact with the E2 and substrate.

Figure 2

Simplified representation of the role of select E3s from Arabidopsis and Oryza Sativa (rice) in regulating nutrient uptake. (A) Under high N, the E3 NLA mediate ubiquitin-dependent degradation of NRT1.7 nitrate transporter to avoid N overaccumulation. The transreceptor NRT1.1B recruits the E3 NBIP1, which ubiquitinates SPX4 allowing the transcription factor NLP3 to enter the nucleus and promote expression of N-responsive genes. (B) Under Pi replete conditions, E3 NLA ubiquitinates PHT1 inorganic phosphate transporters facilitating degradation by the 26S proteasome to reduce uptake and prevent Pi overaccumulation. Under P limiting stress conditions, E3s SDEL1 and SDEL2 mediate the degradation of SPX4, which allows the transcription factor PHR1/2 to activate the expression of PSI genes such as PHT1. Also, the E3 PRU1 mediates degradation of the repressor WRKY6, which relives inhibition of PHO1 transcription. Increase in PHO1 transporter abundance promotes loading of Pi into the root xylem.